Dataset Information

On the need for bundle-specific microstructure kernels in diffusion MRI.

ABSTRACT: Probing microstructure with diffusion magnetic resonance imaging (dMRI) on a scale orders of magnitude below the imaging resolution relies on biophysical modelling of the signal response in the tissue. The vast majority of these biophysical models of diffusion in white matter assume that the measured dMRI signal is the sum of the signals emanating from each of the constituent compartments, each of which exhibits a distinct behaviour in the b-value and/or orientation domain. Many of these models further assume that the dMRI behaviour of the oriented compartments (e.g. the intra-axonal space) is identical between distinct fibre populations, at least at the level of a single voxel. This implicitly assumes that any potential biological differences between fibre populations are negligible, at least as far as is measurable using dMRI. Here, we validate this assumption by means of a voxel-wise, model-free signal decomposition that, under the assumption above and in the absence of noise, is shown to be rank-1. We evaluate the effect size of signal components beyond this rank-1 representation and use permutation testing to assess their significance. We conclude that in the healthy adult brain, the dMRI signal is adequately represented by a rank-1 model, implying that biologically more realistic, but mathematically more complex fascicle-specific microstructure models do not capture statistically significant or anatomically meaningful structure, even in extended high-b diffusion MRI scans.

SUBMITTER: Christiaens D

PROVIDER: S-EPMC7014821 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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On the need for bundle-specific microstructure kernels in diffusion MRI.

Christiaens Daan D Veraart Jelle J Cordero-Grande Lucilio L Price Anthony N AN Hutter Jana J Hajnal Joseph V JV Tournier J-Donald JD

NeuroImage 20191214

Probing microstructure with diffusion magnetic resonance imaging (dMRI) on a scale orders of magnitude below the imaging resolution relies on biophysical modelling of the signal response in the tissue. The vast majority of these biophysical models of diffusion in white matter assume that the measured dMRI signal is the sum of the signals emanating from each of the constituent compartments, each of which exhibits a distinct behaviour in the b-value and/or orientation domain. Many of these models ...[more]

PMID: 31843710

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Project description:Advances in biophysical multi-compartment modeling for diffusion MRI (dMRI) have gained popularity because of greater specificity than DTI in relating the dMRI signal to underlying cellular microstructure. A large range of these diffusion microstructure models have been developed and each of the popular models comes with its own, often different, optimization algorithm, noise model and initialization strategy to estimate its parameter maps. Since data fit, accuracy and precision is hard to verify, this creates additional challenges to comparability and generalization of results from diffusion microstructure models. In addition, non-linear optimization is computationally expensive leading to very long run times, which can be prohibitive in large group or population studies. In this technical note we investigate the performance of several optimization algorithms and initialization strategies over a few of the most popular diffusion microstructure models, including NODDI and CHARMED. We evaluate whether a single well performing optimization approach exists that could be applied to many models and would equate both run time and fit aspects. All models, algorithms and strategies were implemented on the Graphics Processing Unit (GPU) to remove run time constraints, with which we achieve whole brain dataset fits in seconds to minutes. We then evaluated fit, accuracy, precision and run time for different models of differing complexity against three common optimization algorithms and three parameter initialization strategies. Variability of the achieved quality of fit in actual data was evaluated on ten subjects of each of two population studies with a different acquisition protocol. We find that optimization algorithms and multi-step optimization approaches have a considerable influence on performance and stability over subjects and over acquisition protocols. The gradient-free Powell conjugate-direction algorithm was found to outperform other common algorithms in terms of run time, fit, accuracy and precision. Parameter initialization approaches were found to be relevant especially for more complex models, such as those involving several fiber orientations per voxel. For these, a fitting cascade initializing or fixing parameter values in a later optimization step from simpler models in an earlier optimization step further improved run time, fit, accuracy and precision compared to a single step fit. This establishes and makes available standards by which robust fit and accuracy can be achieved in shorter run times. This is especially relevant for the use of diffusion microstructure modeling in large group or population studies and in combining microstructure parameter maps with tractography results.

Project description:In diffusion MRI analysis, advances in biophysical multi-compartment modeling have gained popularity over the conventional Diffusion Tensor Imaging (DTI), because they can obtain a greater specificity in relating the dMRI signal to underlying cellular microstructure. Biophysical multi-compartment models require a parameter estimation, typically performed using either the Maximum Likelihood Estimation (MLE) or the Markov Chain Monte Carlo (MCMC) sampling. Whereas, the MLE provides only a point estimate of the fitted model parameters, the MCMC recovers the entire posterior distribution of the model parameters given in the data, providing additional information such as parameter uncertainty and correlations. MCMC sampling is currently not routinely applied in dMRI microstructure modeling, as it requires adjustment and tuning, specific to each model, particularly in the choice of proposal distributions, burn-in length, thinning, and the number of samples to store. In addition, sampling often takes at least an order of magnitude, more time than non-linear optimization. Here we investigate the performance of the MCMC algorithm variations over multiple popular diffusion microstructure models, to examine whether a single, well performing variation could be applied efficiently and robustly to many models. Using an efficient GPU-based implementation, we showed that run times can be removed as a prohibitive constraint for the sampling of diffusion multi-compartment models. Using this implementation, we investigated the effectiveness of different adaptive MCMC algorithms, burn-in, initialization, and thinning. Finally we applied the theory of the Effective Sample Size, to the diffusion multi-compartment models, as a way of determining a relatively general target for the number of samples needed to characterize parameter distributions for different models and data sets. We conclude that adaptive Metropolis methods increase MCMC performance and select the Adaptive Metropolis-Within-Gibbs (AMWG) algorithm as the primary method. We furthermore advise to initialize the sampling with an MLE point estimate, in which case 100 to 200 samples are sufficient as a burn-in. Finally, we advise against thinning in most use-cases and as a relatively general target for the number of samples, we recommend a multivariate Effective Sample Size of 2,200.

Project description:Non-invasive estimation of brain microstructure features using diffusion MRI (dMRI)-known as Microstructure Imaging-has become an increasingly diverse and complicated field over the last decades. Multi-compartment (MC)-models, representing the measured diffusion signal as a linear combination of signal models of distinct tissue types, have been developed in many forms to estimate these features. However, a generalized implementation of MC-modeling as a whole, providing deeper insights in its capabilities, remains missing. To address this fact, we present Diffusion Microstructure Imaging in Python (Dmipy), an open-source toolbox implementing PGSE-based MC-modeling in its most general form. Dmipy allows on-the-fly implementation, signal modeling, and optimization of any user-defined MC-model, for any PGSE acquisition scheme. Dmipy follows a "building block"-based philosophy to Microstructure Imaging, meaning MC-models are modularly constructed to include any number and type of tissue models, allowing simultaneous representation of a tissue's diffusivity, orientation, volume fractions, axon orientation dispersion, and axon diameter distribution. In particular, Dmipy is geared toward facilitating reproducible, reliable MC-modeling pipelines, often allowing the whole process from model construction to parameter map recovery in fewer than 10 lines of code. To demonstrate Dmipy's ease of use and potential, we implement a wide range of well-known MC-models, including IVIM, AxCaliber, NODDI(x), Bingham-NODDI, the spherical mean-based SMT and MC-MDI, and spherical convolution-based single- and multi-tissue CSD. By allowing parameter cascading between MC-models, Dmipy also facilitates implementation of advanced approaches like CSD with voxel-varying kernels and single-shell 3-tissue CSD. By providing a well-tested, user-friendly toolbox that simplifies the interaction with the otherwise complicated field of dMRI-based Microstructure Imaging, Dmipy contributes to more reproducible, high-quality research.

Dataset Information

On the need for bundle-specific microstructure kernels in diffusion MRI.

Publications

On the need for bundle-specific microstructure kernels in diffusion MRI.

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