Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI

NeuroImage

Volumn 112, Issue , 2015, Pages 278-287

  Pruim, Raimon H R ^a,b   Mennes, Maarten ^a,b   Buitelaar, Jan K ^a,b,c   Beckmann, Christian F ^a,b,d  

^a RADBOUD UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Artifact; Connectivity; Functional MRI; Independent component analysis; Motion; Resting state

Indexed keywords

ADULT; ALGORITHM; ANATOMY AND HISTOLOGY; ARTIFACT; CHILD; FACTUAL DATABASE; HUMAN; IMAGE PROCESSING; MOTION; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; REGRESSION ANALYSIS; REST; STATISTICS AND NUMERICAL DATA;

ADULT; ALGORITHMS; ARTIFACTS; CHILD; DATABASES, FACTUAL; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MOTION; NEURAL PATHWAYS; PRINCIPAL COMPONENT ANALYSIS; REGRESSION ANALYSIS; REST;

EID: 84933037997     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.02.063     Document Type: Article

References (63)

1. Andersson J.L., Jenkinson M., Smith S. Non-linear registration, aka spatial normalisation. Technical Report 2007, FMRIB Centre, Oxford, United Kingdom.
2. Beall E.B., Lowe M.J. SimPACE: generating simulated motion corrupted BOLD data with synthetic-navigated acquisition for the development and evaluation of SLOMOCO: a new, highly effective slicewise motion correction. NeuroImage 2014, 101:21-34.
3. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 2005, 360:1001-1013.
4. Beckmann C., Mackay C., Filippini N., Smith S. Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. NeuroImage 2009, 47:S148.
5. Behzadi Y., Restom K., Liau J., Liu T.T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 2007, 37:90-101.
6. Bhaganagarapu K., Jackson G.D., Abbott D.F. An automated method for identifying artifact in independent component analysis of resting-state FMRI. Front. Hum. Neurosci. 2013, 7:343.
7. Biswal B.B., Mennes M., Zuo X.N., Gohel S., Kelly C., Smith S.M., Beckmann C.F., Adelstein J.S., Buckner R.L., Colcombe S., Dogonowski A.M., Ernst M., Fair D., Hampson M., Hoptman M.J., Hyde J.S., Kiviniemi V.J., Kötter R., Li S.J., Lin C.P., Lowe M.J., Mackay C., Madden D.J., Madsen K.H., Margulies D.S., Mayberg H.S., McMahon K., Monk C.S., Mostofsky S.H., Nagel B.J., Pekar J.J., Peltier S.J., Petersen S.E., Riedl V., Rombouts S.A.R.B., Rypma B., Schlaggar B.L., Schmidt S., Seidler R.D., Siegle G.J., Sorg C., Teng G.J., Veijola J., Villringer A., Walter M., Wang L., Weng X.C., Whitfield-Gabrieli S., Williamson P., Windischberger C., Zang Y.F., Zhang H.Y., Castellanos F.X., Milham M.P. Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4734-4739.
8. Courchesne E., Pierce K. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr. Opin. Neurobiol. 2005, 15:225-230.
9. Couvy-Duchesne B., Blokland G.A.M., Hickie I.B., Thompson P.M., Martin N.G., de Zubicaray G.I., McMahon K.L., Wright M.J. Heritability of head motion during resting state functional MRI in 462 healthy twins. NeuroImage 2014, 102(Pt 2):424-434.
10. Damoiseaux J.S., Rombouts S.A.R.B., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
11. De Martino F., Gentile F., Esposito F., Balsi M., Di Salle F., Goebel R., Formisano E. Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers. NeuroImage 2007, 34:177-194.
12. Dosenbach N.U.F., Nardos B., Cohen A.L., Fair D.A., Power J.D., Church J.A., Nelson S.M., Wig G.S., Vogel A.C., Lessov-Schlaggar C.N., Barnes K.A., Dubis J.W., Feczko E., Coalson R.S., Pruett J.R., Barch D.M., Petersen S.E., Schlaggar B.L. Prediction of individual brain maturity using fMRI. Science (New York, N.Y.) 2010, 329:1358-1361.
13. Fair D.A., Dosenbach N.U.F., Church J.A., Cohen A.L., Brahmbhatt S., Miezin F.M., Barch D.M., Raichle M.E., Petersen S.E., Schlaggar B.L. Development of distinct control networks through segregation and integration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13507-13512.
14. Fair D.A., Cohen A.L., Dosenbach N.U.F., Church J.A., Miezin F.M., Barch D.M., Raichle M.E., Petersen S.E., Schlaggar B.L. The maturing architecture of the brain's default network. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4028-4032.
15. Fair D.A., Cohen A.L., Power J.D., Dosenbach N.U.F., Church J.A., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional brain networks develop from a "local to distributed" organization. PLoS Comput. Biol. 2009, 5:e1000381.
16. Filippini N., MacIntosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7209-7214.
17. Friston K.J., Williams S., Howard R., Frackowiak R.S., Turner R. Movement-related effects in fMRI time-series. Magn. Reson. Med. 1996, 35:346-355.
18. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. NeuroImage 2009, 48:63-72.
19. Griffanti L., Salimi-Khorshidi G., Beckmann C.F., Auerbach E.J., Douaud G., Sexton C.E., Zsoldos E., Ebmeier K.P., Filippini N., Mackay C.E., Moeller S., Xu J., Yacoub E., Baselli G., Ugurbil K., Miller K.L., Smith S.M. ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging. NeuroImage 2014, 95:232-247.
20. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001, 5:143-156.
21. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002, 17:825-841.
22. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
23. Jo H.J., Gotts S.J., Reynolds R.C., Bandettini P.A., Martin A., Cox R.W., Saad Z.S. Effective preprocessing procedures virtually eliminate distance-dependent motion artifacts in resting state FMRI. J. Appl. Math. 2013, 2013:1-17.
24. Kalcher K., Boubela R.N., Huf W., Bartova L., Kronnerwetter C., Derntl B., Pezawas L., Filzmoser P., Nasel C., Moser E. The spectral diversity of resting-state fluctuations in the human brain. PLoS One 2014, 9:e93375.
25. Kelly A.M.C., Di Martino A., Uddin L.Q., Shehzad Z., Gee D.G., Reiss P.T., Margulies D.S., Castellanos F.X., Milham M.P. Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cereb Cortex (New York, N.Y.: 1991) 2009, 19:640-657.
26. Kochiyama T., Morita T., Okada T., Yonekura Y., Matsumura M., Sadato N. Removing the effects of task-related motion using independent-component analysis. NeuroImage 2005, 25:802-814.
27. Kong X.Z., Zhen Z., Li X., Lu H.H., Wang R., Liu L., He Y., Zang Y., Liu J. Individual differences in impulsivity predict head motion during magnetic resonance imaging. PLoS One 2014, 9:e104989.
28. Kundu P., Inati S.J., Evans J.W., Luh W.M., Bandettini P.A. Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI. NeuroImage 2012, 60:1759-1770.
29. Lemieux L., Salek-Haddadi A., Lund T.E., Laufs H., Carmichael D. Modelling large motion events in fMRI studies of patients with epilepsy. Magn. Reson. Imaging 2007, 25:894-901.
30. Liao X.H., Xia M.R., Xu T., Dai Z.J., Cao X.Y., Niu H.J., Zuo X.N., Zang Y.F., He Y. Functional brain hubs and their test-retest reliability: a multiband resting-state functional MRI study. NeuroImage 2013, 83:969-982.
31. Muschelli J., Nebel M.B., Caffo B.S., Barber A.D., Pekar J.J., Mostofsky S.H. Reduction of motion-related artifacts in resting state fMRI using aCompCor. NeuroImage 2014, 96:22-35.
32. Niazy R.K., Xie J., Miller K., Beckmann C.F., Smith S.M. Spectral characteristics of resting state networks. Prog. Brain Res. 2011, 193:259-276.
33. Patel A.X., Kundu P., Rubinov M., Jones P.S., Vértes P.E., Ersche K.D., Suckling J., Bullmore E.T. A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series. NeuroImage 2014, 95:287-304.
34. Perlbarg V., Bellec P., Anton J.L., Pélégrini-Issac M., Doyon J., Benali H. CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. Magn. Reson. Imaging 2007, 25:35-46.
35. Power J.D., Fair D.A., Schlaggar B.L., Petersen S.E. The development of human functional brain networks. Neuron 2010, 67:735-748.
36. 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.
37. 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.
38. Pruim R.H.R., Mennes M., van Rooij D., Llera A., Buitelaar J.K., Beckmann C.F. ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. NeuroImage. 2015, (in press). 10.1016/j.neuroimage.2015.02.064.
39. Pujol J., Macià D., Blanco-Hinojo L., Martínez-Vilavella G., Sunyer J., de la Torre R., Caixàs A., Martín-Santos R., Deus J., Harrison B.J. Does motion-related brain functional connectivity reflect both artifacts and genuine neural activity?. NeuroImage 2014, 101:87-95.
40. Rummel C., Verma R.K., Schöpf V., Abela E., Hauf M., Berruecos J.F.Z., Wiest R. Time course based artifact identification for independent components of resting-state FMRI. Front. Hum. Neurosci. 2013, 7:214.
41. Salimi-Khorshidi G., Douaud G., Beckmann C.F., Glasser M.F., Griffanti L., Smith S.M. Automatic denoising of functional MRI data: combining independent component analysis and hierarchical fusion of classifiers. NeuroImage 2014, 90:449-468.
42. 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.
43. 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.
44. Satterthwaite T.D., Wolf D.H., Ruparel K., Erus G., Elliott M.A., Eickhoff S.B., Gennatas E.D., Jackson C., Prabhakaran K., Smith A., Hakonarson H., Verma R., Davatzikos C., Gur R.E., Gur R.C. Heterogeneous impact of motion on fundamental patterns of developmental changes in functional connectivity during youth. NeuroImage 2013, 83:45-57.
45. Shehzad Z., Kelly A.M.C., Reiss P.T., Gee D.G., Gotimer K., Uddin L.Q., Lee S.H., Margulies D.S., Roy A.K., Biswal B.B., Petkova E., Castellanos F.X., Milham M.P. The resting brain: unconstrained yet reliable. Cereb. Cortex 2009, 19:2209-2229.
46. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
47. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
48. Sochat V., Supekar K., Bustillo J., Calhoun V., Turner J.A., Rubin D.L. A robust classifier to distinguish noise from fMRI independent components. PLoS One 2014, 9:e95493.
49. Spisák T., Jakab A., Kis S.A., Opposits G., Aranyi C., Berényi E., Emri M. Voxel-wise motion artifacts in population-level whole-brain connectivity analysis of resting-state fMRI. PLoS One 2014, 9:e104947.
50. Storti S.F., Formaggio E., Nordio R., Manganotti P., Fiaschi A., Bertoldo A., Toffolo G.M. Automatic selection of resting-state networks with functional magnetic resonance imaging. Front. Neurosci. 2013, 7:72.
51. The ADHD-200 Consortium The ADHD-200 consortium: a model to advance the translational potential of neuroimaging in clinical neuroscience. Front. Syst. Neurosci. 2012, 6:62.
52. Thomas C.G., Harshman R.A., Menon R.S. Noise reduction in BOLD-based fMRI using component analysis. NeuroImage 2002, 17:1521-1537.
53. Tohka J., Foerde K., Aron A.R., Tom S.M., Toga A.W., Poldrack R.A. Automatic independent component labeling for artifact removal in fMRI. NeuroImage 2008, 39:1227-1245.
54. Van De Ven V.G., Formisano E., Prvulovic D., Roeder C.H., Linden D.E.J. Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest. Hum. Brain Mapp. 2004, 22:165-178.
55. Van Dijk K.R.A., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010, 103:297-321.
56. 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.
57. von Rhein D., Mennes M., van Ewijk H., Groenman A.P., Zwiers M.P., Oosterlaan J., Heslenfeld D., Franke B., Hoekstra P.J., Faraone S.V., Hartman C., Buitelaar J. The NeuroIMAGE study: a prospective phenotypic, cognitive, genetic and MRI study in children with attention-deficit/hyperactivity disorder. Design and descriptives. Eur. Child Adolesc. Psychiatry 2015, 24:265-281.
58. Wisner K.M., Atluri G., Lim K.O., Macdonald A.W. Neurometrics of intrinsic connectivity networks at rest using fMRI: retest reliability and cross-validation using a meta-level method. NeuroImage 2013, 76:236-251.
59. Woolrich M.W., Jbabdi S., Patenaude B., Chappell M., Makni S., Behrens T., Beckmann C., Jenkinson M., Smith S.M. Bayesian analysis of neuroimaging data in FSL. NeuroImage 2009, 45:S173-S186.
60. 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.
61. Zeng L.L., Wang D., Fox M.D., Sabuncu M., Hu D., Ge M., Buckner R.L., Liu H. Neurobiological basis of head motion in brain imaging. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6058-6062.
62. Zuo X.N., Xing X.X. Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Neurosci. Biobehav. Rev. 2014, 45:100-118.
63. Zuo X.N., Kelly C., Adelstein J.S., Klein D.F., Castellanos F.X., Milham M.P. Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. NeuroImage 2010, 49:2163-2177.