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Correction of artefacts in simultaneous multi-slice multi-PLD arterial spin labelling data using Gaussian Process regression
Jack Toner1,2, Flora Kennedy McConnell1,2,3, Yuriko Suzuki4, Timothy S. Coalson5, Michael P. Harms6, Matthew F. Glasser5,7, and Michael A. Chappell1,2,3,4
1Radiological Sciences, Mental Health & Clinical Neurosciences, School of Medicine, University of Nottingham, Nottingham, United Kingdom, 2Sir Peter Mansfield Imaging Centre, School of Medicine, University of Nottingham, Nottingham, United Kingdom, 3Nottingham Biomedical Research Centre, Queens Medical Centre, University of Nottingham, Nottingham, United Kingdom, 4Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom, 5Department of Neuroscience, Washington University School of Medicine, St Louis, MO, United States, 6Department of Psychiatry, Washington University School of Medicine, St Louis, MO, United States, 7Department of Radiology, Washington University School of Medicine, St Louis, MO, United States

Synopsis

Simultaneous multi-slice (SMS) acquisitions enable higher resolutions to be achieved for arterial spin labelling (ASL) images. However, SMS acquisitions can introduce a banded pattern of intensity within the images. This reduces the quality of motion estimation as the algorithm aligns the bands in preference to the brain structures. We introduce a Gaussian Process model that can be used to correct the banding in SMS multiple post-labelling delay ASL data, which should improve motion correction. We demonstrate its effectiveness on 10 subjects from the Human Connectome Project Aging dataset. We anticipate that the model will generalise to other ASL datasets.

Introduction

Simultaneous multi-slice arterial spin labelling (SMS-ASL) acquisitions enable higher resolutions to be achieved for ASL images, such as those acquired by the Human Connectome Project (HCP) Aging and Development studies.1 However, the acquisitions can lead to sharp discontinuities in intensity between slices in different bands, particularly when physically adjacent slices are acquired serially in time. Motion estimates are then degraded as the algorithm aligns the bands in preference to brain structures, preventing effective motion correction.2 Gaussian processes have been used to improve motion estimation in diffusion MRI with severe distortion artefacts.3,4 We introduce a Gaussian Process (GP) model, used as part of the process to correct the artefacts in SMS-ASL multiple post-labelling delay (multi-PLD) data. We demonstrate its effectiveness on 10 subjects from the HCP Aging (HCP-A) study where two effects interact to produce discontinuities.

Methods

We introduce an algorithm which models how SMS-ASL multi-PLD non-background suppressed signal varies with partial volume estimates (PVEs), slice number and PLD. We obtain 2 predictions: the model’s prediction of the original image with banding and its prediction of the corrected image. We then use the ratio between these 2 predictions to correct the original image.
Instead of using a fully deterministic model, we use a GP where our mean function is the product of a constant, $$$c$$$ , and a saturation recovery term:
$$m\left(\mathbf{x}\right)=c\times\left[ p_{gm}M_{0_{gm}}\left(1-e^{-\frac{t}{T_{1_{gm}}}}\right)+p_{wm}M_{0_{wm}}\left(1-e^{-\frac{t}{T_{1_{wm}}}}\right)+p_{csf}M_{0_{csf}}\left(1-e^{-\frac{t}{T_{1_{csf}}}}\right)\right]$$
$$$\mathbf{x}$$$ is the voxel's $$$5\times1$$$ feature vector and $$$p_{tissue}$$$ are the PVEs at the voxel. $$$c$$$, $$$M_{0_{tissue}}$$$ and $$$T_{1_{tissue}}$$$ are hyperparameters to be estimated. Our covariance function is:
$$K\left(\mathbf{x},\mathbf{x'};\mathbf{\Omega},v,l\right)=k_{pve}\left(\mathbf{p},\mathbf{p'};\mathbf{\Omega}\right)\times\left(k_{slice}\left(s,s';v\right)+k_t\left(t,t';l\right)\right)$$
$$K\left(\mathbf{x},\mathbf{x'};\mathbf{\Omega},v,l\right)=exp\left(-\frac{1}{2}\left(\mathbf{p}-\mathbf{p'}\right)^T\mathbf{\Omega}^{-1}\left(\mathbf{p}-\mathbf{p'}\right)\right)\times\left(\left(v\times s\times s'\right)+exp\left(-\frac{\left(t-t'\right)^2}{l^2}\right)\right)$$
$$$\mathbf{p}$$$ is a $$$3\times1$$$ vector of PVEs, $$$s$$$ is the position of the voxel in a band, $$$t$$$ is the PLD and the hyperparameters $$$\mathbf{\Omega}$$$, $$$v$$$ and $$$l$$$ are lengthscales which determine how the predictions vary in feature space.

The HCP-A ASL data consists of 43 label-control pairs at 5 PLDs (0.2s, 0.7s, 1.2s, 1.7s, 2.2s), labelling duration of 1.5s, varying numbers of repeats (6, 6, 6, 10, 15 respectively), 2.5mm isotropic resolution, 60 slices acquired with 6-fold acceleration (slice readout time of 0.059s). Two M0 images (TR>8s) were acquired at the same spatial resolution. Two reversed phase-encoded spin-echo images were processed using TOPUP for susceptibility distortion correction.5 Correction for gradient nonlinearity was also performed. T1 and T2-weighted structural images (0.8mm isotropic resolution) were processed using FreeSurfer.1,6 PVEs were obtained in ASL native space using Toblerone.7 Motion estimation was performed using FSL mcflirt (first M0 image as reference image).8 Registration to structural space was performed using FreeSurfer’s bbregister.9 Receive-coil bias correction was applied using sensitivity maps estimated from a grey matter mask in the first M0 image.
The GP’s hyperparameters are optimised on a subject-specific basis. 200 voxels are sampled from the first (control) image at each PLD and M0 image, totalling 1200 training points, with 10% of the voxels within the ventricular CSF mask. During model prediction, at each voxel, the data from the 43 control volumes and the 2 M0 images are used alongside the training data.

Results

We observe 2 effects in the HCP-A data which interact to produce the banding visible in Figure 1. The first, believed to be a magnetisation transfer (MT) effect, is visible in Figures 1a and 1b and causes signal intensity to decrease as slice number increases. Figure 2 shows this effect is approximately linear within the data and stronger in white matter than in grey matter. The second, the saturation recovery effect, causes signal intensity to increase with PLD. This is most pronounced at PLD=0.2s because the slice readout time is largest relative to the nominal PLD. The two effects largely cancel out at this PLD, resulting in less obvious discontinuities in Figure 1c.
Figures 3a-c show predictions from the GP which has learned the data’s signal variation with PLD. Figure 3d shows the model learns that signal varies linearly with slice number and that the effect is stronger in white matter than in grey matter, as seen in Figure 2.
Figure 4 shows the discontinuities in mean slicewise signal are reduced after correction compared to Figure 2, indicating the approximately linear trend with slice number is alleviated.
Figure 5 shows the ratio of the GP’s predictions visibly removes the banding pattern, particularly at later PLDs.

Discussion

This work introduced a GP which models SMS-ASL multi-PLD signal as a function of PVEs, slice number and PLD. Predictions from the GP corrected the banding in HCP-A data and we expect this will result in improved motion correction and a reduction in artefacts. We anticipate this will generalise to other SMS-ASL datasets, including SMS acquisitions with background suppression. The correction was less effective at early PLDs where banding is less substantial, even before correction. Figure 5d shows the GP produces low predictions of CSF signal at earlier PLDs, resulting in suppressed CSF signal in the corrected images.

Conclusion

The GP successfully corrects artefacts in non-background suppressed, SMS-ASL multi-PLD data on a subject-specific basis, particularly at later PLDs. It is expected to generalise to other ASL datasets. Further work is required to improve the correction at earlier PLDs and in CSF.

Acknowledgements

JT and MAC have received support from the Engineering and Physical Sciences Research Council UK (EP/P012361/1). FKM is supported by the Beacon of Excellence in Precision Imaging, University of Nottingham. YS is supported by the Royal Academy of Engineering under the Research Fellowship scheme (RF/201920/19/236) and core funding from the Wellcome Trust (203139/Z/16/Z). MPH is supported by grants: U01MH109589 and U01AG052564. MFG is supported by grants: R24MH108315 and R24MH122820.

References

1. Harms, Michael P., et al. "Extending the Human Connectome Project across ages: Imaging protocols for the Lifespan Development and Aging projects." Neuroimage 183 (2018): 972-984.

2. Suzuki, Yuriko, et al. "A framework for motion correction of background suppressed arterial spin labeling perfusion images acquired with simultaneous multi‐slice EPI." Magnetic resonance in medicine 81.3 (2019): 1553-1565.

3. Andersson, Jesper LR, and Stamatios N. Sotiropoulos. "An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging." Neuroimage 125 (2016): 1063-1078.

4. Andersson, Jesper LR, and Stamatios N. Sotiropoulos. "Non-parametric representation and prediction of single-and multi-shell diffusion-weighted MRI data using Gaussian processes." Neuroimage 122 (2015): 166-176.

5. Andersson, Jesper LR, Stefan Skare, and John Ashburner. "How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging." Neuroimage 20.2 (2003): 870-888.

6. Glasser, Matthew F., et al. "The minimal preprocessing pipelines for the Human Connectome Project." Neuroimage 80 (2013): 105-124.

7. Kirk, Thomas F., et al. "Toblerone: surface-based partial volume estimation." IEEE transactions on medical imaging 39.5 (2019): 1501-1510.

8. Jenkinson, Mark, et al. "Improved optimization for the robust and accurate linear registration and motion correction of brain images." Neuroimage 17.2 (2002): 825-841.

9. Greve, Douglas N., and Bruce Fischl. "Accurate and robust brain image alignment using boundarybased registration." Neuroimage 48.1 (2009): 63-72.

Figures

Figure 1. Examples of distortion- and receive-coil bias-corrected images from HCP-A. Two opposing effects are present in the images: the first, believed to be an MT effect, causes signal to decrease as slice number increases, while a saturation recovery effect works in an opposite direction to increase signal with slice number. At long TRs (a) or PLDs (b), the saturation recovery effect is minimal so the first effect is clearly visible. For short PLDs (c) the saturation recovery effect is stronger and counteracts the first effect, so the banding pattern is less obvious.

Figure 2. Slicewise mean signal in grey and white matter tissue masks applied to the distortion- and bias-corrected M0 images of 10 HCP-A subjects. Grey and white matter masks were obtained by thresholding the respective PVEs at 70% and 90% respectively. Linear trends were fit on data from slices 10-49. Signal decreases with increasing slice number within the 2 tissues. The effect is stronger in white matter, evidenced by the larger discontinuities at the band boundaries in white matter.

Figure 3. (a), (b) and (c) show the observed and predicted signal for a range of acquisition times in a CSF, WM and GM/CSF partial-volumed voxel respectively. Solid lines represent the GP’s mean prediction and shaded regions represent the GP’s 95% confidence regions. The GP’s predictions are in good agreement with the observations. (d) shows the learned signal variation with slice number. This is linear and the learned trend is stronger in WM than in GM, as was observed in the data in Figure 2.

Figure 4. Slicewise mean signal in grey and white tissue masks, pre-correction (solid line and circle points, this is the same as Figure 2) and post-correction (dashed line and cross points), for (a) one subject, (b) population of 10 subjects. The discontinuities at the band boundaries are alleviated, both for the subject-specific case (a) and the population-averaged case (b).

Figure 5. Example predictions from the GP and corrected images for 1 HCP-A subject: (a), (e), (I) show receive-coil bias- and distortion-corrected data from PLD=0.2s, PLD=2.2s and M0 images respectively; (b), (f), (j) show the GP’s predictions of these images; (c), (g), (k) show the GP’s predictions of the images with the banding removed; (d), (h), (l) show the corrected images. The banding is removed at later PLDs (h) while still visible at the earliest PLDs (d).

Proc. Intl. Soc. Mag. Reson. Med. 30 (2022)
0909
DOI: https://doi.org/10.58530/2022/0909