Prospective motion correction with volumetric navigators (vNavs) reduces the bias and variance in brain morphometry induced by subject motion

NeuroImage

Volumn 127, Issue , 2016, Pages 11-22

  Tisdall, M Dylan ^a   Reuter, Martin ^a,d   Qureshi, Abid ^a   Buckner, Randy L ^a,b,c   Fischl, Bruce ^a,d   van der Kouwe, André J W ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bias; Cortical gray matter estimates; Head motion; Motion correction; MRI; Quality control; Thickness; Volume

Indexed keywords

ACCELERATION; ADULT; ARTICLE; ARTIFACT; BIOSENSOR; BRAIN MORPHOMETRY; BRAIN SIZE; COMPUTER PROGRAM; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); EFFECT SIZE; FEMALE; GLUCOSE SENSOR; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; IMAGE QUALITY; MALE; MORPHOMETRICS; MOTION; MOTION CORRECTION; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; VOLUMETRIC NAVIGATOR; ALGORITHM; BRAIN; HEAD MOVEMENT; IMAGE PROCESSING; PROCEDURES; YOUNG ADULT;

ADULT; ALGORITHMS; ARTIFACTS; BRAIN; FEMALE; HEAD MOVEMENTS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MOTION; NEUROIMAGING; YOUNG ADULT;

EID: 84955063528     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.11.054     Document Type: Article

References (42)

1. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851. 10.1016/j.neuroimage.2005.02.018.
2. Bates D.M. Lme4: Mixed-effects modeling with R (January 11, 2010 draft) [WWW Document] URL, (accessed 3.25.15). https://r-forge.r-project.org/scm/viewvc.php/*checkout*/www/lMMwR/lrgprt.pdf?revision=600&root=lme4.
3. Bates D., Mächler M., Bolker B., Walker S. Fitting Linear Mixed-Effects Models using lme4 (stat). arxiv:1406.5823.
4. Benner T., Wisco J.J., van der Kouwe A.J.W., Fischl B., Vangel M.G., Hochberg F.H., Sorensen A.G. Comparison of manual and automatic section positioning of brain MR images. Radiology 2006, 239:246-254. 10.1148/radiol.2391050221.
5. Brown T.T., Kuperman J.M., Erhart M., White N.S., Roddey J.C., Shankaranarayanan A., Han E.T., Rettmann D., Dale A.M. Prospective motion correction of high-resolution magnetic resonance imaging data in children. NeuroImage 2010, 53:139-145. 10.1016/j.neuroimage.2010.06.017.
6. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. NeuroImage 1999, 9:195-207. 10.1006/nimg.1998.0396.
7. Fischl B., Sereno M.I., Tootell R.B., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 1999, 8:272-284. 10.1002/(SICI)1097-0193(1999)8:4<272::AID-HBM10>3.0.CO;2-4.
8. Fitzmaurice G.M., Laird N.M., Ware J.H. Applied longitudinal analysis 2012, John Wiley & Sons.
9. Gaser C. Voxel-based Morphometry Extension to SPM8 [WWW Document] URL. http://dbm.neuro.uni-jena.de/vbm/.
10. Han X., Jovicich J., Salat D., van der Kouwe A., Quinn B., Czanner S., Busa E., Pacheco J., Albert M., Killiany R., Maguire P., Rosas D., Makris N., Dale A., Dickerson B., Fischl B. Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. NeuroImage 2006, 32:180-194. 10.1016/j.neuroimage.2006.02.051.
11. Harvard Center for Brain Science Quality Control [WWW Document] URL, (accessed 2.4.15). http://cbs.fas.harvard.edu/science/core-facilities/neuroimaging/information-investigators/qc.
12. Hess A.T., Tisdall M.D., Andronesi O.C., Meintjes E.M., van der Kouwe A.J.W. Real-time motion and B0 corrected single voxel spectroscopy using volumetric navigators. Magn. Reson. Med. 2011, 66:314-323. 10.1002/mrm.22805.
13. Hess A.T., van der Kouwe A.J.W., Mbugua K.K., Laughton B., Meintjes E.M. Quality of 186 child brain spectra using motion and B0 shim navigated single voxel spectroscopy. J. Magn. Reson. Imaging 2014, 40:958-965. 10.1002/jmri.24436.
14. Jenkinson M. Measuring transformation error by RMS deviation. Technical Report No. TR99MJ1 1999, FMRIB, Oxford.
15. Koldewyn K., Yendiki A., Weigelt S., Gweon H., Julian J., Richardson H., Malloy C., Saxe R., Fischl B., Kanwisher N. Differences in the right inferior longitudinal fasciculus but no general disruption of white matter tracts in children with autism spectrum disorder. Proc. Natl. Acad. Sci. 2014, 111:1981-1986. 10.1073/pnas.1324037111.
16. Kuperman J.M., Brown T.T., Ahmadi M.E., Erhart M.J., White N.S., Roddey J.C., Shankaranarayanan A., Han E.T., Rettmann D., Dale A.M. Prospective motion correction improves diagnostic utility of pediatric MRI scans. Pediatr. Radiol. 2011, 41:1578-1582. 10.1007/s00247-011-2205-1.
17. Maclaren J., Herbst M., Speck O., Zaitsev M. Prospective motion correction in brain imaging: a review. Magn. Reson. Med. 2013, 69:621-636. 10.1002/mrm.24314.
18. Maclaren J., Han Z., Vos S.B., Fischbein N., Bammer R. Reliability of brain volume measurements: a test-retest datase. Sci. Data 2014, 1:140037. 10.1038/sdata.2014.37.
19. Mugler J.P., Brookeman J.R. Three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE). Magn. Reson. Med. 1990, 15:152-157. 10.1002/mrm.1910150117.
20. Mugler J.P., Brookeman J.R. Rapid three-dimensional T1-weighted MR imaging with the MP-RAGE sequence. J. Magn. Reson. Imaging 1991, 1:561-567. 10.1002/jmri.1880010509.
21. North B.V., Curtis D., Sham P.C. A note on the calculation of empirical P values from Monte Carlo procedures. Am. J. Hum. Genet. 2002, 71:439-441. 10.1086/34152710.1086/341527.
22. Ooi M.B., Krueger S., Thomas W.J., Swaminathan S.V., Brown T.R. Prospective real-time correction for arbitrary head motion using active markers. Magn. Reson. Med. 2009, 62:943-954. 10.1002/mrm.22082.
23. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 2012, 59:2142-2154. 10.1016/j.neuroimage.2011.10.018.
24. Power J.D., Mitra A., Laumann T.O., Snyder A.Z., Schlaggar B.L., Petersen S.E. Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 2014, 84:320-341. 10.1016/j.neuroimage.2013.08.048.
25. Qureshi A.Y., Mueller S., Snyder A.Z., Mukherjee P., Berman J.I., Roberts T.P.L., Nagarajan S.S., Spiro J.E., Chung W.K., Sherr E.H., Buckner R.L. Opposing brain differences in 16p11.2 deletion and duplication carriers. J. Neurosci. 2014, 34:11199-11211. 10.1523/JNEUROSCI.1366-14.2014.
26. Reuter M., Rosas H.D., Fischl B. Highly accurate inverse consistent registration: a robust approach. NeuroImage 2010, 53:1181-1196. 10.1016/j.neuroimage.2010.07.020.
27. Reuter M., Schmansky N.J., Rosas H.D., Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 2012, 61:1402-1418. 10.1016/j.neuroimage.2012.02.084.
28. Reuter M., Tisdall M.D., Qureshi A., Buckner R.L., van der Kouwe A.J.W., Fischl B. Head motion during MRI acquisition reduces gray matter volume and thickness estimates. NeuroImage 2015, 107:107-115. 10.1016/j.neuroimage.2014.12.006.
29. Satterthwaite T.D., Wolf D.H., Loughead J., Ruparel K., Elliott M.A., Hakonarson H., Gur R.C., Gur R.E. Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth. NeuroImage 2012, 60:623-632. 10.1016/j.neuroimage.2011.12.063.
30. Satterthwaite T.D., Elliott M.A., Gerraty R.T., Ruparel K., Loughead J., Calkins M.E., Eickhoff S.B., Hakonarson H., Gur R.C., Gur R.E., Wolf D.H. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage 2013, 64:240-256. 10.1016/j.neuroimage.2012.08.052.
31. Thesen S., Heid O., Mueller E., Schad L.R. Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magn. Reson. Med. 2000, 44:457-465. 10.1002/1522-2594(200009)44:3<457::AID-MRM17>3.0.CO;2-R.
32. Tisdall M.D., Hess A.T., Reuter M., Meintjes E.M., Fischl B., van der Kouwe A.J.W. Volumetric navigators for prospective motion correction and selective reacquisition in neuroanatomical MRI. Magn. Reson. Med. 2012, 68:389-399. 10.1002/mrm.23228.
33. van der Kouwe A.J.W., Benner T., Fischl B., Schmitt F., Salat D.H., Harder M., Sorensen A.G., Dale A.M. On-line automatic slice positioning for brain MR imaging. NeuroImage 2005, 27:222-230. 10.1016/j.neuroimage.2005.03.035.
34. van der Kouwe A.J.W., Benner T., Dale A.M. Real-time rigid body motion correction and shimming using cloverleaf navigators. Magn. Reson. Med. 2006, 56:1019-1032. 10.1002/mrm.21038.
35. van der Kouwe A.J.W., Benner T., Salat D.H., Fischl B. Brain morphometry with multiecho MPRAGE. NeuroImage 2008, 40:559-569. 10.1016/j.neuroimage.2007.12.025.
36. Van Dijk K.R.A., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 2012, 59:431-438. (Neuroergonomics: The human brain in action and at work). 10.1016/j.neuroimage.2011.07.044.
37. White N., Roddey C., Shankaranarayanan A., Han E., Rettmann D., Santos J., Kuperman J., Dale A. PROMO: real-time prospective motion correction in MRI using image-based tracking. Magn. Reson. Med. 2010, 63:91-105. 10.1002/mrm.22176.
38. Wolfram Research Inc. Mathematica, Version 10.0 2014, Wolfram Research, Inc., Champaign, Illinois, (ed).
39. Yan C.-G., Cheung B., Kelly C., Colcombe S., Craddock R.C., Di Martino A., Li Q., Zuo X.-N., Castellanos F.X., Milham M.P. A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. NeuroImage 2013, 76:183-201. 10.1016/j.neuroimage.2013.03.004.
40. Yendiki A., Koldewyn K., Kakunoori S., Kanwisher N., Fischl B. Spurious group differences due to head motion in a diffusion MRI study. NeuroImage 2014, 88:79-90. 10.1016/j.neuroimage.2013.11.027.
41. Zaitsev M., Dold C., Sakas G., Hennig J., Speck O. Magnetic resonance imaging of freely moving objects: Prospective real-time motion correction using an external optical motion tracking system. NeuroImage 2006, 31:1038-1050. 10.1016/j.neuroimage.2006.01.039.
42. Zaitsev M., Maclaren J., Herbst M. Motion artifacts in MRI: a complex problem with many partial solutions. J. Magn. Reson. Imaging 2015, (n/a-n/a). 10.1002/jmri.2485010.1002/jmri.24850.