Decoding the microstructural properties of white matter using realistic models

Hédouin, Renaud; Metere, Riccardo; Chan, Kwok‐Shing; Licht, Christian; Mollink, Jeroen; Walsum, Anne‐Marie van Cappellen van; Marques, José P.

doi:10.1016/j.neuroimage.2021.118138

Cited by 16 publications

(23 citation statements)

References 57 publications

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“…A14 in ( 16)). Interestingly, the realistic geometry of the WM fibre also plays an important role in the compartmental frequency shifts (27,44). This effect is clearly illustrated in the frequency perturbation simulations in The enhanced R1 in deep GM suggests the contribution of iron to the R1 was more pronounced.…”

Section: Discussionmentioning

confidence: 87%

“…A14 in (16)). Interestingly, the realistic geometry of the WM fibre also plays an important role in the compartmental frequency shifts (27,44). This effect is clearly illustrated in the frequency perturbation simulations in Figure 5: not only the centres but also the FWHM of the extra-cellular frequency distribution of the two samples are different, despite the two specimens having virtually identical MVF and AVF.…”

Section: Discussionmentioning

confidence: 99%

“…The experiment consisted of two imaging sessions: the first session was conducted on the whole-brain specimen and the second session was conducted on the excised brain tissues. The following protocol was used for the first session: MP2RAGE adopted to sensitise for T 1 values between 250 ms and 1000 ms, 1 mm isotropic resolution, TI1/TI2/TR=311/1600/3000 ms, flip angle ( α ) #1/#2 = 4°/6°, Tacq = 5 min; 2D spin-echo EPI DWI, 1.6 mm isotropic, TR/TE=15241/77.6 ms, 2-shell (b=0/1250/2500 s/mm 2 , 17/120/120 measurements with 7 b=0 measurements collected with reversed phase-encode blips for distortion correction), 20 repetitions, Tacq = 5.6 hours; Monopolar, 3D multi-echo GRE, 1 mm isotropic resolution, TR/TE1/ΔTE/TE6=40/3.45/6.27/34.8 ms, α =20° (optimised for WM T 1 ), 10 orientations with respect to B 0 , chosen to optimise microstructural information decoding (27); Tacq = 1.7 hours. …”

Section: Methodsmentioning

confidence: 99%

“…Monopolar, 3D multi-echo GRE, 1 mm isotropic resolution, TR/TE1/ΔTE/TE6=40/3.45/6.27/34.8 ms, α =20° (optimised for WM T 1 ), 10 orientations with respect to B 0 , chosen to optimise microstructural information decoding (27); Tacq = 1.7 hours.…”

Section: Methodsmentioning

confidence: 99%

“…Effective axonal diameter was defined as the square root of the product of the 2 nd and 3 rd principal axis lengths of the axons obtained from the regionprop3 function of MATLAB (Mathworks, Natick, US), from which the median and the skewness of the axonal diameter distribution were computed. Fibre dispersion was computed from the axonal volume-weighted average squared dot product between the axon main principal direction and the average orientation of the entire sample (27). To further investigate the effect of realistic myelin sheath geometry on the compartmental frequency shifts, field perturbations induced from myelin χ i was simulated in two scenarios: when the segmented sample axons were parallel or perpendicular to B 0 .…”

Section: Methodsmentioning

confidence: 99%

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Studying magnetic susceptibility, microstructural compartmentalisation and chemical exchange in a formalin-fixed ex vivo human brain specimen

Chan

Hédouin

Mollink

et al. 2021

Preprint

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Purpose: Ex vivo imaging is a preferable method to study the biophysical mechanism of white matter orientation-dependent signal phase evolution. Yet, how formalin fixation, commonly used for tissue preservation, affects the phase measurement is not fully known. We, therefore, study the impacts of formalin fixation on magnetic susceptibility, microstructural compartmentalisation and chemical exchange measurement on human brain tissue. Methods: A formalin-fixed, post-mortem human brain specimen was scanned with multiple orientations with respect to the main magnetic field direction for robust bulk magnetic susceptibility measurement with conventional quantitative susceptibility imaging models. Homogeneous white matter tissues were subsequently excised from the whole-brain specimen and scanned in multiple rotations on an MRI scanner to measure the anisotropic magnetic susceptibility and microstructure-related contributions in the signal phase. Electron microscopy was used to validate the MRI findings. Results: The bulk isotropic magnetic susceptibility of ex vivo whole-brain imaging is comparable to in vivo imaging, with noticeable enhanced non-susceptibility contributions. The excised specimen experiment reveals that anisotropic magnetic susceptibility and compartmentalisation phase effect were considerably reduced in formalin-fixed white matter tissue. Conclusions: Despite formalin-fixed white matter tissue has comparable bulk isotropic magnetic susceptibility to those measured via in vivo imaging, its orientation-dependent components in the signal phase related to the tissue microstructure is substantially weaker, making it less favourable in white matter microstructure studies using phase imaging.

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Section: Discussionmentioning

confidence: 87%

“…A14 in (16)). Interestingly, the realistic geometry of the WM fibre also plays an important role in the compartmental frequency shifts (27,44). This effect is clearly illustrated in the frequency perturbation simulations in Figure 5: not only the centres but also the FWHM of the extra-cellular frequency distribution of the two samples are different, despite the two specimens having virtually identical MVF and AVF.…”

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 3 more Smart Citations

Studying magnetic susceptibility, microstructural compartmentalisation and chemical exchange in a formalin-fixed ex vivo human brain specimen

Chan

Hédouin

Mollink

et al. 2021

Preprint

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Imaging white matter microstructure with gradient‐echo phase imaging: Is ex vivo imaging with formalin‐fixed tissue a good approximation of the in vivo brain?

Chan

Hédouin

Mollink

et al. 2022

Magnetic Resonance in Med

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Purpose Ex vivo imaging is a commonly used approach to investigate the biophysical mechanism of orientation‐dependent signal phase evolution in white matter. Yet, how phase measurements are influenced by the structural alteration in the tissue after formalin fixation is not fully understood. Here, we study the effects on magnetic susceptibility, microstructural compartmentalization, and chemical exchange measurement with a postmortem formalin‐fixed whole‐brain human tissue. Methods A formalin‐fixed, postmortem human brain specimen was scanned with multiple orientations to the main magnetic field direction for robust bulk magnetic susceptibility measurement with conventional quantitative susceptibility imaging models. White matter samples were subsequently excised from the whole‐brain specimen and scanned in multiple rotations on an MRI scanner to measure the anisotropic magnetic susceptibility and microstructure‐related contributions in the signal phase and to validate the findings of the whole‐brain data. Results The bulk isotropic magnetic susceptibility of ex vivo whole‐brain imaging is comparable to in vivo imaging, with noticeable enhanced nonsusceptibility contributions. The excised specimen experiment reveals that anisotropic magnetic susceptibility and compartmentalization phase effect were considerably reduced in the formalin‐fixed white matter specimens. Conclusions Formalin‐fixed postmortem white matter exhibits comparable isotropic magnetic susceptibility to previous in vivo imaging findings. However, the measured phase and magnitude data of the fixed white matter tissue shows a significantly weaker orientation dependency and compartmentalization effect. Alternatives to formalin fixation are needed to better reproduce the in vivo microstructural effects in postmortem samples.

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Incorporating the effect of white matter microstructure in the estimation of magnetic susceptibility in ex vivo mouse brain

Sandgaard,

Kiselev,

Henriques

et al. 2023

Magnetic Resonance in Med

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PurposeTo extend quantitative susceptibility mapping to account for microstructure of white matter (WM) and demonstrate its effect on ex vivo mouse brain at 16.4T.Theory and MethodsPrevious studies have shown that the MRI measured Larmor frequency also depends on local magnetic microstructure at the mesoscopic scale. Here, we include effects from WM microstructure using our previous results for the mesoscopic Larmor frequency of cylinders with arbitrary orientations. We scrutinize the validity of our model and QSM in a digital brain phantom including from a WM susceptibility tensor and biologically stored iron with scalar susceptibility. We also apply susceptibility tensor imaging to the phantom and investigate how the fitted tensors are biased from . Last, we demonstrate how to combine multi‐gradient echo and diffusion MRI images of ex vivo mouse brains acquired at 16.4T to estimate an apparent scalar susceptibility without sample rotations.ResultsOur new model improves susceptibility estimation compared to QSM for the brain phantom. Applying susceptibility tensor imaging to the phantom with from WM axons with scalar susceptibility produces a highly anisotropic susceptibility tensor that mimics results from previous susceptibility tensor imaging studies. For the ex vivo mouse brain we find the due to WM microstructure to be substantial, changing susceptibility in WM up to 25% root‐mean‐squared‐difference.Conclusion impacts susceptibility estimates and biases susceptibility tensor imaging fitting substantially. Hence, it should not be neglected when imaging structurally anisotropic tissue such as brain WM.

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Decoding the microstructural properties of white matter using realistic models

Cited by 16 publications

References 57 publications

Studying magnetic susceptibility, microstructural compartmentalisation and chemical exchange in a formalin-fixed ex vivo human brain specimen

Studying magnetic susceptibility, microstructural compartmentalisation and chemical exchange in a formalin-fixed ex vivo human brain specimen

Imaging white matter microstructure with gradient‐echo phase imaging: Is ex vivo imaging with formalin‐fixed tissue a good approximation of the in vivo brain?

Incorporating the effect of white matter microstructure in the estimation of magnetic susceptibility in ex vivo mouse brain

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