Evaluating BOLD functional MRI biophysical simulation approaches: Impact of vascular geometry, magnetic field calculations, and water diffusion models

Abstract Biophysical simulations have guided the development of blood oxygenation level-dependent (BOLD) functional MRI (fMRI) acquisitions and signal models that relate the BOLD signal to the underlying physiology, such as calibrated BOLD and vascular fingerprinting. Numerous simulation techniques have been developed, however, few of them have been directly compared, thus limiting the assessment of the accuracy and interchangeability of these methods as well as the accuracy of the quantitative techniques derived from them. In this work, we compared the accuracy and computational demands of eight previously published simulation approaches that adopt different geometries (ranging from infinite cylinders to synthetic vascular anatomical networks (VANs)), field offset calculations (analytical and Fourier-based), and water diffusion implementations (Monte Carlo and convolution-based), all of which are available in an open-source Python toolkit, BOLDsωimsuite. The reference simulation approach for comparison used three-dimensional infinite cylinders, analytical field offsets, and Monte Carlo diffusion. When compared with the reference approach, most of the simulations, including two- and three-dimensional geometries, were in excellent agreement when assuming the intravascular signal contribution was small. Two commonly employed simulation approaches were notably biased; both used two-dimensional geometries with overly simplified vasculature or field offset calculations. In general, the simulated intravascular signal was the least consistent across approaches, thus potentially resulting in larger errors when the intravascular signal contribution is large. Lastly, the VAN results were in good agreement with the reference but they diverged slightly, yet systematically, from each other at smaller radii (≲3 μm), primarily driven by intravascular signal differences. We conclude, therefore, that the reference approach is an attractive option for exploratory simulations in the many cases where anatomical and haemodynamic realism is not needed, balancing ease of implementation, accessibility, versatility, computational efficiency, accuracy of results, and interpretability. These findings help pave the way for a broader adoption of forward modelling of the BOLD signal and more reliable interpretations of biophysical simulations aiming to develop quantitative models of the BOLD signal.

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