Viscoelastic properties of the ferret brain measured in vivo at multiple frequencies by magnetic resonance elastography

Feng, Yuan; Clayton, Erik H.; Chang, Yulin V.; Okamoto, Ruth J.; Bayly, Philip V.

doi:10.1016/j.jbiomech.2012.12.024

Cited by 67 publications

(67 citation statements)

References 46 publications

(76 reference statements)

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“…Recent indentation tests have shown that gray and white matter display rather similar stiffnesses, both of the order of 1kPa [11]. These values agree with recent in vivo measurements using magnetic resonance elastography [16]. Introducing white matter growth makes cortical folding possible, even for small stiffness contrasts [5].…”

Section: Discussionsupporting

confidence: 76%

Emerging Brain Morphologies from Axonal Elongation

2015

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Understanding the characteristic morphology of our brain remains a challenging, yet important task in human evolution, developmental biology, and neurosciences. Mathematical modeling shapes our understanding of cortical folding and provides functional relations between cortical wavelength, thickness, and stiffness. Yet, current mathematical models are phenomenologically isotropic and typically predict non-physiological, periodic folding patterns. Here we establish a mechanistic model for cortical folding, in which macroscopic changes in white matter volume are a natural consequence of microscopic axonal growth. To calibrate our model, we consult axon elongation experiments in chick sensory neurons. We demonstrate that a single parameter, the axonal growth rate, explains a wide variety of in vitro conditions including immediate axonal thinning and gradual thickness restoration. We embed our axonal growth model into a continuum model for brain development using axonal orientation distributions motivated by diffusion spectrum imaging. Our simulations suggest that white matter anisotropy - as an emergent property from directional axonal growth - intrinsically induces symmetry breaking, and predicts more physiological, less regular morphologies with regionally varying gyral wavelengths and sulcal depths. Mechanistic modeling of brain development could establish valuable relationships between brain connectivity, brain anatomy, and brain function.

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Section: Discussionsupporting

confidence: 76%

Emerging Brain Morphologies from Axonal Elongation

2015

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“…Magnetic resonance elastography measures the mechanical properties of soft tissues by introducing shear waves and assessing their propagation velocity using magnetic resonance imaging. A recent study in ferrets suggested that, at loading rates from 400Hz to 800Hz, elastic and viscous properties of gray and white matter were indistinguishable [12]. Another study in humans at loading rates of 200Hz found that gray matter storage moduli, with 3.1kPa, were on average 12% larger than white matter storage moduli, with 2.7kPa, while loss moduli of gray and white matter, with 2.5kPa, were identical [21].…”

Section: Discussionmentioning

confidence: 99%

“…While five decades of research have generated a profound understanding of brain tissue as a whole [7], the individual rheology of gray and white matter remains understudied and poorly understood. As a result of inconsistent sample preparation, post-mortem time, and testing conditions, reported stiffness values are often irreproducible and may vary by an order of magnitude or more [35]: Some studies reported that gray matter was substantially stiffer than white matter [9], others found that they were of equal stiffness [12], and yet others observed that white matter was stiffer [45]. Here, to address this discrepancy, we adopt a robust, reliable, and repeatable method to quantify the mechanical properties of gray and white matter, flat-punch indentation.…”

Section: Motivationmentioning

confidence: 99%

Mechanical properties of gray and white matter brain tissue by indentation

Budday

Nay

Rooij

et al. 2015

Journal of the Mechanical Behavior of Biomedical Materials

536

451

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The mammalian brain is composed of an outer layer of gray matter, consisting of cell bodies, dendrites, and unmyelinated axons, and an inner core of white matter, consisting primarily of myelinated axons. Recent evidence suggests that microstructural differences between gray and white matter play an important role during neurodevelopment. While brain tissue as a whole is rheologically well characterized, the individual features of gray and white matter remain poorly understood. Here we quantify the mechanical properties of gray and white matter using a robust, reliable, and repeatable method, flat-punch indentation. To systematically characterize gray and white matter moduli for varying indenter diameters, loading rates, holding times, post-mortem times, and locations we performed a series of n=192 indentation tests. We found that indenting thick, intact coronal slices eliminates the common challenges associated with small specimens: it naturally minimizes boundary effects, dehydration, swelling, and structural degradation. When kept intact and hydrated, brain slices maintained their mechanical characteristics with standard deviations as low as 5% throughout the entire testing period of five days post mortem. White matter, with an average modulus of 1.895kPa±0.592kPa, was on average 39% stiffer than gray matter, p<0.01, with an average modulus of 1.389kPa±0.289kPa, and displayed larger regional variations. It was also more viscous than gray matter and responded less rapidly to mechanical loading. Understanding the rheological differences between gray and white matter may have direct implications on diagnosing and understanding the mechanical environment in neurodevelopment and neurological disorders.

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“…Riek et al (2011) reported that G′ of a gelatin gel measured by MRE increased with the frequency between 100 and 800 Hz. Feng et al (2013) also measured the G′ and G″ of ferret brains in vivo by MRE in the excitation frequency of 400-800 Hz and that the complex shear modulus increased with the frequency. The viscoelastic modulus of agarose gels was measured using the MRE system under the excitation conditions.…”

Section: Discussionmentioning

confidence: 98%

Viscoelastic modulus of agarose gels by magnetic resonance elastography using Micro-MRI

Suzuki

Tadano

Goto

et al. 2015

Mechanical Engineering Journal

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This study aimed to apply magnetic resonance elastography (MRE) using micro-magnetic resonance imaging (micro-MRI) system for the measurements of viscoelastic modulus in soft matters. The rectangular specimens of 90 × 70 × 50 mm were made of agarose gel with five kinds of stiffness by changing concentrations. The specimens were oscillated with longitudinal waves transmitted by an elastic-bar from a vibration generator in a micro-MRI system. Since the viscoelastic properties depend on the excitation frequency and amplitude, the experimental conditions were selected in the range of 50-250 Hz and 0.1-0.5 mm. The viscoelastic modulus was expressed as storage shear modulus G′ and loss shear modulus G″. As a result, G′ increased with the frequency and amplitude, and the difference of G′ between hard and soft gels was obtained. The viscoelastic modulus of agarose gels was measured using the MRE system under the excitation conditions. Furthermore, double-layer specimens composed of 0.6 and 2.0 wt% gels were examined as an application of the MRE system. The difference of wave pattern between the hard and soft parts was observed. The values of G′ in the soft parts of the double-layer specimens corresponded to the value of the single-layer specimen, but the values of G′ in the hard parts were varied. and Klatt et al. (2010) have also measured the viscoelastic modulus of livers in vivo.The authors developed an MRE system consisting of a micro-magnetic resonance imaging (micro-MRI) with 0.3 T, a bar-type transmitter, and a vibration generator, which allowed the excitation frequency of 50-250 Hz and the amplitude of 0.1-0.5 mm (Tadano, et al., 2012). The bar-type transmitter and the vibration generator were used to generate strong excitation. In that study, it was confirmed that the distribution of displacement was obtained within the agarose gel of 1.2 wt% concentration under the excitation conditions. Furthermore, to decrease the error of viscoelastic modulus, the authors proposed a calculation method for the MRE measurements under the low magnetic field based on the integration of the displacement (Jiang and Nakamura, 2011). It is necessary to apply the MRE instrument and the calculation method to the measurements of viscoelastic modulus of soft matters and to discuss the availability of the system. Therefore, the present study aimed to investigate the effect of the excitation frequency of 50-250 Hz and the amplitude of 0.1-0.5 mm on the viscoelastic modulus of agarose gels with five kinds of stiffness by using the MRE system. Furthermore, the distributions of the displacement and viscoelastic modulus in the specimens consisting of hard and soft gel parts were investigated as an application of the MRE system. Three kinds of the double-layer specimen were examined in the study. MethodsWhen a specimen was excited with a sine wave in the MRI, local displacements in the specimen under a gradient magnetic field were calculated from the phase shift of MR signal (Muthupillai, et al., 1996;Manduca, et al., 2001). A complex...

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Viscoelastic properties of the ferret brain measured in vivo at multiple frequencies by magnetic resonance elastography

Cited by 67 publications

References 46 publications

Emerging Brain Morphologies from Axonal Elongation

Emerging Brain Morphologies from Axonal Elongation

Mechanical properties of gray and white matter brain tissue by indentation

Viscoelastic modulus of agarose gels by magnetic resonance elastography using Micro-MRI

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