Orientation dependence of inhomogeneous magnetization transfer and dipolar order relaxation rate in phospholipid bilayers

Morris, Sarah; Frederick, Rebecca A.; MacKay, Alex L.; Laule, Cornelia; Michal, Carl A.

doi:10.1016/j.jmr.2022.107205

Cited by 10 publications

(18 citation statements)

References 29 publications

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“…In addition to the time dependence of the transverse relaxation function

of the lipid‐bound protons in bilayers, the LDM also predicts the

orientation dependence that is in agreement with experimental data. Indeed, the LDM‐predicted angular dependence of the relaxation function

in flat bilayers (

per Equation ( 31 )) is similar to that found experimentally by Morris et al 48 Indeed, Morris et al measured the orientation dependence of the second moment (M 2 ) of the lineshape in an oriented phospholipid bilayer at 9.4T. They found a strong orientation dependence that was maximized when the bilayers were aligned perpendicular to

and minimized near the magic angle (∼54.7°) and followed an orientation dependence given by the second Legendre polynomial squared.…”

Section: Discussionsupporting

confidence: 85%

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Microscopic theory of spin–spin and spin–lattice relaxation of bound protons in cellular and myelin membranes—A lateral diffusion model (LDM)

Sukstanskiı̆

Yablonskiy

2022

Magnetic Resonance in Med

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Deciphering salient features of biological tissue cellular microstructure in health and diseases is an ultimate goal of MRI. While most MRI approaches are based on studying MR properties of tissue "free" water indirectly affected by tissue microstructure, other approaches, such as magnetization transfer (MT), directly target signals from tissue-forming macromolecules. However, despite three-decades of successful applications, relationships between MT measurements and tissue microstructure remain elusive, hampering interpretation of experimental results. The goal of this paper is to develop microscopic theory connecting the structure of cellular and myelin membranes to their MR properties.Theory and Methods: Herein we introduce a lateral diffusion model (LDM) that explains the T 2 (spin-spin) and T 1 (spin-lattice) MRI relaxation properties of the macromolecular-bound protons by their dipole-dipole interaction modulated by the lateral diffusion of long lipid molecules forming cellular and myelin membranes. Results: LDM predicts anisotropic T 1 and T 2 relaxation of membrane-bound protons. Moreover, their T 2 relaxation cannot be described in terms of a standard R 2 = 1/T 2 relaxation rate parameter, but rather by a relaxation rate function R 2 (t) that depends on time t after RF excitation, having, in the main approximation, a logarithmic behavior: R 2 (t) ∼ lnt. This anisotropic non-linear relaxation leads to an absorption lineshape that is different from Super-Lorentzian traditionally used in interpreting MT experiments. Conclusion: LDM-derived analytical equations connect the membrane-boundprotons T 1 and T 2 relaxation with dynamic distances between protons in neighboring membrane-forming lipid molecules and their lateral diffusion. This sheds new light on relationships between MT parameters and microstructure of cellular and myelin membranes.

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“…In addition to the time dependence of the transverse relaxation function

of the lipid‐bound protons in bilayers, the LDM also predicts the

orientation dependence that is in agreement with experimental data. Indeed, the LDM‐predicted angular dependence of the relaxation function

in flat bilayers (

and minimized near the magic angle (∼54.7°) and followed an orientation dependence given by the second Legendre polynomial squared.…”

Section: Discussionsupporting

confidence: 85%

“…per Equation ( 31)) is similar to that found experimentally by Morris et al 48 Indeed, Morris et al measured the orientation dependence of the second moment (M 2 )…”

Section: Discussionsupporting

confidence: 85%

Microscopic theory of spin–spin and spin–lattice relaxation of bound protons in cellular and myelin membranes—A lateral diffusion model (LDM)

Sukstanskiı̆

Yablonskiy

2022

Magnetic Resonance in Med

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“…In a previous study, we found the changing linewidth to be the dominant mechanism determining ihMTR orientation dependence in a lipid bilayer sample under our experimental conditions. 17 However, the apparent orientation dependence of ihMTR in the healthy adult brain did not match this in vitro work. We believe that the discrepancy is due to a combination of the chosen ihMT frequency offset changing the apparent orientation dependence curve and also the natural heterogeneity of myelin across the brain.…”

Section: Discussionmentioning

confidence: 70%

“…11 It has also been found to vary significantly with fiber orientation in white matter in vivo and in a phospholipid bilayer model-likely due to the oriented nature of dipolar coupling in the myelin bilayers that wrap around axons. 12,17,18 Myelin water imaging (MWI) is another MRI method that is sensitive to myelin. This method isolates the short T 2 signal from water trapped between myelin bilayers.…”

Section: Introductionmentioning

confidence: 99%

Myelin biomarkers in the healthy adult brain: Correlation, reproducibility, and the effect of fiber orientation

Morris

Vavasour

Smolina

et al. 2022

Magnetic Resonance in Med

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We investigated the correlation, reproducibility, and effect of white matter fiber orientation for three myelin-sensitive MRI techniques: magnetization transfer ratio (MTR), inhomogeneous magnetization transfer ratio (ihMTR), and gradient and spin echo-derived myelin water fraction (MWF). Methods: We measured the three metrics in 17 white and three deep grey matter regions in 17 healthy adults at 3 T. Results:We found a strong correlation between ihMTR and MTR (r = 0.70, p < 0.001) and ihMTR and MWF (r = 0.79, p < 0.001), and a weaker correlation between MTR and MWF (r = 0.54, p < 0.001). The dynamic range in white matter was greatest for MWF (2.0%-27.5%), followed by MTR (14.4%-23.2%) and then ihMTR (1.2%-5.4%). The average scan-rescan coefficient of variation for white matter regions was 0.6% MTR, 0.3% ihMTR, and 0.7% MWF in metric units; however, when adjusted by the dynamic range, these became 6.3%, 6.1% and 2.8%, respectively. All three metrics varied with fiber direction: MWF and ihMTR were lower in white matter fibers perpendicular to B 0 by 6% and 1%, respectively, compared with those parallel, whereas MTR was lower by 0.5% at about 40 • , with the highest values at 90 • . However, separating the apparent orientation dependence by white matter region revealed large dissimilarities in the trends, suggesting that real differences in myelination between regions are confounding the apparent orientation dependence measured using this method. Conclusion:The strong correlation between ihMTR and MWF suggests that these techniques are measuring the same myelination; however, the larger dynamic range of MWF may provide more power to detect small differences in myelin.

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“…Although the nerve fiber orientation effects on T2 relaxation are weaker than the effects on T2* ( Kaczmarz et al, 2020 ), GRASE-based MWF was found to vary by approximately 35% for different white matter fiber orientations and to generally decrease with increasing fiber angles ( Birkl et al, 2021 ). While MT parameters such as the apparent transverse relaxation constant of the semisolid pool have revealed similar orientation dependence with peak values around 30° - 50° and decreasing values with higher fiber angles ( Pampel et al, 2015 ), ihMTR values were found to be maximized for fibers perpendicular to the main magnetic field ( Girard et al, 2017 ; Morris et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Comparing myelin-sensitive magnetic resonance imaging measures and resulting g-ratios in healthy and multiple sclerosis brains

et al. 2022

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Orientation dependence of inhomogeneous magnetization transfer and dipolar order relaxation rate in phospholipid bilayers

Cited by 10 publications

References 29 publications

Microscopic theory of spin–spin and spin–lattice relaxation of bound protons in cellular and myelin membranes—A lateral diffusion model (LDM)

Microscopic theory of spin–spin and spin–lattice relaxation of bound protons in cellular and myelin membranes—A lateral diffusion model (LDM)

Myelin biomarkers in the healthy adult brain: Correlation, reproducibility, and the effect of fiber orientation

Comparing myelin-sensitive magnetic resonance imaging measures and resulting g-ratios in healthy and multiple sclerosis brains

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