Myung-Ho In1, Daehun Kang1, Hang Joon Jo2, Uten Yarach3, Joshua D Trzasko1, Nolan K Meyer1,4, Bardwell Speltz J Lydia 1,4, John Huston III1, Matt A Bernstein1, and Yunhong Shu1
1Department of Radiology, Mayo Clinic, Rochester, MN, United States, 2Department of Physiology, College of Medicine, Hanyang University, Seoul, Korea, Republic of, 3Department of Radiologic Technology, Faculty of Associated Medical Sciences, Chiang Mai University, Chiang Mai, Thailand, 4Mayo Clinic Graduate School of Biomedical Sciences, Mayo Clinic, Rochester, MN, United States
Synopsis
Interleaved reverse-gradient fMRI
(RG-fMRI) with a PSF mapping-based distortion correction scheme has the potential
to minimize the loss of signal in regions of rapid susceptibility change. Recently,
multi-band imaging was combined to improve the temporal resolution for RG-fMRI,
and the initial feasibility was
evaluated in human. In this
work, breath-holding task-fMRI was performed with the proposed scheme to demonstrate
the effectiveness in improving fMRI reliability for each individual and the
entire group, especially in high susceptibility brain regions.
Introduction
A PSF-mapping-based reverse-gradient (PSF-RG)
approach can minimize susceptibility-induced artifacts by correcting geometric distortion
in a pair of echo-planar-imaging (EPI) data with opposite phase-encoding (PE)
gradient polarities and combining them. The efficiency was previously demonstrated
in pig’s brain for fMRI during deep-brain-stimulation.1 Initial feasibility for whole-brain human fMRI was tested after adopting multi-band
imaging to improve the temporal resolution.2 In this work, breath-holding task-based fMRI was
performed in healthy volunteers with the proposed acquisition and correction
scheme. fMRI reliability improvements were
evaluated for both each individual and at the group level, especially in brain
regions of high susceptibility.Methods
After informed consent, breath-holding functional MRI (fMRI) was
performed in six healthy volunteers using a 32-channel coil (Nova Medical, USA)
on a compact 3T scanner with high-performance gradients (700 T/ms/s, 80 mT/m),3-5
with negligible peripheral nerve stimulation.6 The block
paradigm consisted of 5 rest (20 s) and breath-holding (20 s) cycles and ended
with a rest period. The PE polarity in each EPI repetition was altered in an
interleaved order for the reverse gradient fMRI (RG-fMRI). The imaging
protocols were: TR/TE = 1000/30 ms, no partial Fourier, multi-band factor = 6,
79 slices, 2 mm isotropic resolution. Before RG-fMRI scan, a PSF mapping scan
with the reverse PE polarity1,7 was performed
for distortion calibration with identical imaging parameters as the fMRI,
except for TR/TE = 934/24.4 ms. The scan time for fMRI and calibration were 3
minutes 50 seconds and 34 seconds, respectively. Additionally, an anatomical T1
image was obtained with the following parameters: TR/TE/TI = 6/2.5/900 ms, flip
angle = 8°, and 1 mm isotropic resolution.
After the PSF-based EPI distortion
correction,1,7 three
different variants of the EPI series including: the distortion-corrected forward
and reverse EPIs (DF and DR), and the weighted combination of the
distortion-corrected EPI pair (DW) were generated. Co-registration between the
functional and the anatomical images with rigid body transform using AFNI
software8 was conducted. Segmentation
and parcellation of anatomical images were performed using FreeSurfer.9 For the surface-based
group comparison, each cortical boundary derived by FreeSurfer was used to convert
functional data onto a 3D standard-mesh cortical surface model.10,11
General linear model (GLM)-based blood oxygenation level-dependent (BOLD) contrasts
were estimated in each individual and for the entire group.
To evaluate the
improvements associated with the proposed human task-fMRI studies, the image intensity and functional contrasts
in the regions with strong susceptibility artifacts were compared visually and
quantitatively across the three different variants of the EPI series. Two-way
ANOVA was applied to compare three different variants of the EPI series. To
clearly demonstrate the improvements in local BOLD contrasts arising from the
improved signal redistribution rather than the increased image SNR due to image
combination, signal percentage changes were calculated which were not dominated
by SNR.1Results and Discussion
With multi-band imaging, the
effective temporal resolution of the RG-fMRI was 2s which can efficiently capture
the BOLD signal change over time. As shown in the distortion-corrected images
(Fig. 1), the susceptibility-induced signal dropout was clearly different
between the forward and reverse EPIs in regions of temporal and frontal lobes
and varied across the slices within the subject, which resulted in mismatched
activation maps in the affected areas (arrows in Fig. 1). When compared to the
EPI pair, more apparent signal dropouts appeared in temporal and frontal lobes,
respectively in the forward and the reverse images (Fig. 1) and the similar
result was observed in the group coverage-ratio map (Fig. 2A). Even with strong
signal dropout of the EPI pair in the regions of temporal lobes, signal loss
was significantly reduced in the combined data as the signal dropout patterns are
different for the forward and the reverse EPI (arrows in Fig. 2A). This
improved both the global group coverage ratio and regional coverage ratio (Fig.
2B). In group level analysis, the GLM-based fMRI t-score map of the DW data is visually
more robust than the t-score maps derived from either the forward or reversion
EPI data (Fig. 3a). In addition, the
overall activation pattern of the t-score maps is very similar to the signal change
percentage map which is relatively independent from the image SNR (Fig. 3b).
Therefore, it was demonstrated that the improvements in local areas of the
group activation map were mainly due to the signal distortion correction,
rather than the SNR improvement in the combination of the EPI pair.Conclusion
This study demonstrates that
the multi-band PSF-based RG approach can be beneficial to improve the fMRI reliability in both individual
and group data analysis, especially in high susceptibility brain regions. Therefore,
the proposed approach represents a viable method for investigating the brain functional
mechanisms in the temporal and frontal areas which have not been intensively explored
yet due to conventional EPI limitation.Acknowledgements
This work was
supported by NIH U01 EB024450 and NHI U01 EB026979. The authors would like to
thank Jennifer Myers and Erin Gray for their help in collecting the data.References
1. In
MH, Cho S, Shu Y, Min HK, Bernstein MA, Speck O, Lee KH, Jo HJ. Correction of
metal-induced susceptibility artifacts for functional MRI during deep brain
stimulation. NeuroImage 2017;158:26-36.
2. In MH, Kang D, Jo HJ, Yarach Y, Meyer NK, Trzasko JD,
Gray EM, Huston J, Bernstein MA, Shu Y. Initial feasibility of a multi-band
PSF-mapping based, reverse-gradient approach with geometric distortion correction
for whole-brain fMRI. 28th scientific meeting of ISMRM 2020:p. 1218.
3. Foo TKF, Laskaris E, Vermilyea M, Xu M, Thompson P,
Conte G, Van Epps C, Immer C, Lee SK, Tan ET, Graziani D, Mathieu JB, Hardy CJ,
Schenck JF, Fiveland E, Stautner W, Ricci J, Piel J, Park K, Hua Y, Bai Y,
Kagan A, Stanley D, Weavers PT, Gray E, Shu Y, Frick MA, Campeau NG, Trzasko J,
Huston J, 3rd, Bernstein MA. Lightweight, compact, and high-performance 3T MR
system for imaging the brain and extremities. Magn Reson Med 2018;80(5):2232-2245.
4. Lee SK, Mathieu JB, Graziani D, Piel J, Budesheim E,
Fiveland E, Hardy CJ, Tan ET, Amm B, Foo TKF. Peripheral nerve stimulation
characteristics of an asymmetric head‐only gradient coil
compatible with a high‐channel‐count receiver array. Magnetic
resonance in medicine 2016;76(6):1939-1950.
5. Weavers PT, Shu Y, Tao S, Huston J, Lee SK, Graziani D,
Mathieu JB, Trzasko JD, Foo TKF, Bernstein MA. Compact three‐tesla
magnetic resonance imager with high‐performance gradients passes
ACR image quality and acoustic noise tests. Medical physics
2016;43(3):1259-1264.
6. In MH, Shu Y, Trzasko JD, Yarach U, Kang D, Gray EM,
Huston J, Bernstein MA. Reducing PNS with minimal performance penalties via
simple pulse sequence modifications on a high-performance compact 3T scanner.
Physics in Medicine & Biology 2020;65(15):15NT02.
7. In MH, Posnansky O, Beall EB, Lowe MJ, Speck O.
Distortion correction in EPI using an extended PSF method with a reversed phase
gradient approach. PLoS ONE 2015;10(2):e0116320.
8. Cox RW. AFNI: software for analysis and visualization
of functional magnetic resonance neuroimages. Comput Biomed Res
1996;29(3):162-173.
9. Reuter M, Schmansky NJ, Rosas HD, Fischl B.
Within-subject template estimation for unbiased longitudinal image analysis.
Neuroimage 2012;61(4):1402-1418.
10. Kang D, Jo HJ, In MH, Y Uten, Meyer NK, Bardwell Speltz LJ, Gray EM, Trzasko JD, Huston J III, Bernstein MA, Y Shu. The benefit of high-performance gradient
on echo planar imaging for BOLD-based resting-state functional MRI. Physics in
Medicine & Biology 2020.
11. Saad ZS, Reynolds RC, Argall B, Japee S, Cox RW. SUMA: an
interface for surface-based intra-and inter-subject analysis with AFNI. 2004.
IEEE. p 1510-1513.