Malte Hoffmann1,2, Robert Frost1,2, David Salat1,2, M Dylan Tisdall3, Jonathan Polimeni1,2, and André van der Kouwe1,2
1Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, MA, United States, 2Department of Radiology, Harvard Medical School, Boston, MA, United States, 3Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
Synopsis
Volumetric navigators (vNavs) interleaved within longer MRI
sequences are an effective method for dynamically detecting and correcting head
motion during the acquisition. However, motion is estimated by registering each
vNav back to the first, and bias can be introduced by non-rigid deformations of,
e.g., the mouth, since the head is taken to be a rigid body. We demonstrate
that this bias introduces correction-related artifacts. We present robust real-time
brain extraction (0.02 s per vNav) and demonstrate offline that the bias and
associated artifacts can be removed by using motion tracks from brain-masked
registration.
Introduction
Volumetric navigators1 (vNavs) interleaved within longer
MRI sequences are an effective method for dynamically detecting and correcting head
motion during the acquisition.2 Motion is estimated by
registering each vNav back to the first, assuming all of the anatomy in the
navigator FOV moves rigidly. However, when the navigator FOV encompasses the
entire head, non-rigid deformations, such as opening and closing the mouth, can
bias the detection of brain motion. This leads to incorrect motion "correction"
and ultimately undesired image artifacts.
We present an experiment showing that non-rigid
motion biases the detection and introduces artifacts when the vNav-based motion
estimates are used for correction. To address this, we developed robust
ultra-fast brain extraction targeted to vNavs and demonstrated offline that leveraging
the derived masks for brain-only registration substantially improves the
correction.Methods
Real-time brain extraction
The brain was identified in vNavs (3D EPI, 323
8-mm voxels) as a maximally stable extremal region3 (MSER). We implemented a 3D detector4 to extract global MSERS
offline, i.e. clusters of N voxels at the minimum of their growth rate dN/dI over the entire range of intensities I (8 bits, Δ=127). The
largest MSER was selected and morphologically opened with a spherical kernel of
radius r=3 to remove parts of the neck. A typical vNav and derived mask are
shown in Figure 1.
Evaluation of masking performance
We evaluated the accuracy of our masking procedure in n=258
vNav timeseries from the Human Connectome Project5,6 (HCP-A) using the Dice overlap
metric. We compared the first vNav mask of each series to a down-sampled mask
generated with FreeSurfer7 from the associated
motion-corrected MPRAGE. Consistency across time was assessed by comparing the masks
of each vNav series to its first frame.
Non-rigid head motion experiment
For this study, a subject was instructed to open and close
their mouth at random times during a vNav-MPRAGE acquisition at 3T while
otherwise remaining still (matrix 256×256×176, resolution 1×1×1 mm, TR/TI/TE 2500/1070/2.9 ms, FA 8°, readout
bandwidth 240 Hz/px, GRAPPA R=2). For a fair comparison between registration methods,
Siemens' on-scanner PACE8 algorithm was used to estimate
motion from vNavs without applying real-time corrections to the sequence.
Retrospective motion correction
Brain-masked registration of vNavs was performed
offline using FSL/FLIRT9 with brain masks. For robust registration the
masks were morphologically dilated to include the scalp using a spherical
kernel of radius r=2. RetroMocoBox10 was adapted to perform offline correction and
GRAPPA reconstruction of vNav-MPRAGE k-space datasets based on different motion
traces.Results
Masking performance
Figure 2A
shows the distribution of Dice coefficients D. The overlap
with masks from FreeSurfer was D=0.89±0.01 while the within
time-series consistency was D=0.99±0.02. Typically, a few voxels at the outer
edges of the masks changed labels between consecutive vNav frames (from brain
to non-brain or vice versa) due to noise. Masking took about 0.02 seconds per
vNav on a 3.3-GHz Intel Xeon CPU.
Bias due to non-rigid motion
Figure 3
compares brain-motion estimates in the presence of local deformation. PACE estimated
large head movements at the times the subject was instructed to open and close their
mouth. FLIRT with brain masks detected substantially reduced translations and
almost no rotations. In contrast, PACE also detected drifts in head orientation
over time. FLIRT without masks estimated reduced motion as compared to PACE but
was found to be more sensitive to jaw motion than brain-masked registration.
Retrospective motion correction
T1-weighted images are shown in Figure
4A after retrospective correction with the
motion traces estimated by each algorithm. PACE introduced subtle artifacts
that were removed by brain-specific registration, and this was reflected by
changes in Shannon entropy (n=256 bins, see Figure
2B).Discussion
We demonstrated that non-rigid head motion introduces bias
in the detection of brain motion using vNavs with Siemens' PACE algorithm and
introduces correction-related artifacts. We presented robust ultra-fast brain
extraction from vNavs suitable for real-time use and showed that brain-masked
registration removes the artifacts at 3T.
Further experiments may establish anatomy-specific
registration for vNav-based correction at 7T, where large distortions around
the sinuses are a known source of inaccuracy11. We expect that adapting our approach
to children and infants12 will increase the usefulness
of vNavs, as bias is introduced if the shoulders or chest impinge on the
navigator FOV.
While FLIRT reduced the bias from non-rigid
deformations even without brain masks, we note that its execution time of about
6 seconds per vNavs is incompatible with real-time application during
MPRAGE. Further work is needed to incorporate our brain masks into an optimized
on-scanner registration.Conclusion
We presented enhancements to vNav-based motion
correction using robust real-time brain masking and demonstrated that
brain-specific registration removes correction-related artifacts in the
presence of non-rigid head motion. This may be useful for imaging initiatives
such as ABCD and HCP where subjects are often non-compliant.Acknowledgements
This research was supported by the ABCD-USA
Consortium (U24DA041123) and by NIH grants R00HD074649, U01AG052564 ,
R01HD099846, R01HD093578, R01HD085813.References
1. Tisdall
MD, Hess AT, Reuter M, Meintjes EM, Fischl B, van der Kouwe AJW. Volumetric
navigators for prospective motion correction and selective reacquisition in
neuroanatomical MRI. Magn Reson Med. 2012;68(2):389-399.
2. Tisdall
MD, Reuter M, Qureshi A, Buckner RL, Fischl B, van der Kouwe AJW. Prospective
motion correction with volumetric navigators (vNavs) reduces the bias and
variance in brain morphometry induced by subject motion. Neuroimage.
2016;127:11-22.
3. Matas
J, Chum O, Urban M, Pajdla T. Robust wide-baseline stereo from maximally stable
extremal regions. Image Vis Comput. 2004;22(10):761-767.
4. Kristensen
F, MacLean WJ. Real-Time Extraction of Maximally Stable Extremal Regions on an
FPGA. In: 2007 IEEE International Symposium on Circuits and Systems.
IEEE; 2007:165-168.
5. Harms
MP, Somerville LH, Ances BM, et al. Extending the Human Connectome Project
across ages: Imaging protocols for the Lifespan Development and Aging projects.
Neuroimage. 2018;183:972-984.
6. Bookheimer
SY, Salat DH, Terpstra M, et al. The Lifespan Human Connectome Project in
Aging: An overview. Neuroimage. 2019;185:335-348.
7. Fischl
B. FreeSurfer. Neuroimage. 2012;62(2):774-781.
8. Thesen
S, Heid O, Mueller E, Schad LR. Prospective acquisition correction for head
motion with image-based tracking for real-time fMRI. Magn Reson Med.
2000;44(3):457-465.
9. Jenkinson
M, Smith S. A global optimisation method for robust affine registration of
brain images. Med Image Anal. 2001;5(2):143-156.
10. Gallichan
D, Marques JP, Gruetter R. Retrospective correction of involuntary microscopic
head movement using highly accelerated fat image navigators (3D FatNavs) at 7T.
Magn Reson Med. 2015.
11. Liu J,
de Zwart JA, van Gelderen P, Murphy-Boesch J, Duyn JH. Effect of head motion on
MRI B0 field distribution. Magn Reson Med. 2018;80(6):2538-2548.
12. Brown
TT, Kuperman JM, Erhart M, et al. Prospective motion correction of
high-resolution magnetic resonance imaging data in children. Neuroimage.
2010;53(1):139-145.