Abstract
There is growing awareness that brain mechanical properties are important for neural development and health. However, published values of brain stiffness differ by orders of magnitude between static measurements and in vivo magnetic resonance elastography (MRE), which covers a dynamic range over several frequency decades. We here show that there is no fundamental disparity between static mechanical tests and in vivo MRE when considering large-scale properties, which encompass the entire brain including fluid filled compartments. Using gradient echo real-time MRE, we investigated the viscoelastic dispersion of the human brain in, so far, unexplored dynamic ranges from intrinsic brain pulsations at 1 Hz to ultralow-frequency vibrations at 5, 6.25, 7.8 and 10 Hz to the normal frequency range of MRE of 40 Hz. Surprisingly, we observed variations in brain stiffness over more than two orders of magnitude, suggesting that the in vivo human brain is superviscous on large scales with very low shear modulus of 42±13 Pa and relatively high viscosity of 6.6±0.3 Pa∙s according to the two-parameter solid model. Our data shed light on the crucial role of fluid compartments including blood vessels and cerebrospinal fluid (CSF) for whole brain properties and provide, for the first time, an explanation for the variability of the mechanical brain responses to manual palpation, local indentation, and high-dynamic tissue stimulation as used in elastography.
Highlights
It is a peculiarity of mechanical testing of soft biological tissues, in particular the brain, that there is an obvious discrepancy between local mechanical tests utilizing quasi-static deformations, in vivo properties measured by magnetic resonance elastography (MRE) (1000 to 3500 Pa for the human brain[37, 10,000] to 20,000 Pa for the mouse brain36), and reports of fresh ex vivo brains that have a very low flexural modulus[38] confirmed by our whole brain stiffness measurement that led to a value of 100 Pa
Combining wave profile analysis for extrinsic and intrinsic MRE allowed us to measure the continuous increase in shear wave speed (SWS) of in vivo brain from 0.1 to 1.9m/s
Our results show good reproducibility of ssMRE values for 5 and 10Hz, which are both outside the range that has been explored in vivo so far
Summary
The in-vivo mechanical properties of the brain are increasingly recognized as being tightly linked to neuronal development[1] and aging[2,3], myelination[4], functional activation[5,6], memory performance[7,8], body-mass index 9, and cerebrovascular perfusion 10,11 as well as pathophysiological processes including brain tumor progression[12,13,14,15,16], neuroinflammation[17,18,19], and neuronal dementia[20,21,22,23].Elasticity, stiffness, and rigidity are synonymously used to refer to the major output parameter of clinical elastography, which is directly linked to the lengths of shear waves[24]. Stiffness values can vary by orders of magnitude across testing modes (e.g., stretching vs compression vs shear26,27), models (e.g., linear vs nonlinear, isotropic vs anisotropic28-31), dynamic ranges (e.g., static vs highdynamic32,33), tissue regions (e.g., full brain or white matter vs cortical tissue or deepgray matter34,35), specimens (e.g., human vs mouse brain36,37), or viability status (e.g., in vivo vs in situ, post mortem, or ex vivo38,39) as reported before[25,40]. MRE typically exploits a mechanical frequency range of 30 to 100Hz43 leaving a significant gap of values to quasi-static ex vivo methods
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