Is fMRI "noise" really noise? Resting state nuisance regressors remove variance with network structure

NeuroImage

Volumn 114, Issue , 2015, Pages 158-169

  Bright, Molly G ^a,b,c   Murphy, Kevin ^c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Connectivity; FMRI; Motion; Noise correction; Regression; Resting state

Indexed keywords

ADULT; ARTIFACT; BRAIN; BRAIN MAPPING; FEMALE; HUMAN; MALE; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; REGRESSION ANALYSIS;

ADULT; ARTIFACTS; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; REGRESSION ANALYSIS;

EID: 84937765110     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.03.070     Document Type: Article

References (37)

1. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc., B 2005, 360:1001-1013. 10.1002/(SICI)1097-0193(1999)8:2/3<151::AID-HBM13>3.0.CO;2-5.
2. Birn R.M., Smith M.A., Jones T.B., Bandettini P.A. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage 2008, 40:644-654. 10.1016/j.neuroimage.2007.11.059.
3. Birn R.M., Molloy E.K., Patriat R., Parker T., Meier T.B., Kirk G.R., Nair V.A., Meyerand M.E., Prabhakaran V. The effect of scan length on the reliability of resting-state fMRI connectivity estimates. NeuroImage 2013, 83:550-558. 10.1016/j.neuroimage.2013.05.099.
4. Bright M.G., Murphy K. Removing motion and physiological artifacts from intrinsic BOLD fluctuations using short echo data. NeuroImage 2013, 64:526-537. 10.1016/j.neuroimage.2012.09.043.
5. Bright M.G., Murphy K. Reliable quantification of BOLD fMRI cerebrovascular reactivity despite poor breath-hold performance. NeuroImage 2013, 83C:559-568. 10.1016/j.neuroimage.2013.07.007.
6. Bright M.G., Bulte D.P., Jezzard P., Duyn J.H. Characterization of regional heterogeneity in cerebrovascular reactivity dynamics using novel hypocapnia task and BOLD fMRI. NeuroImage 2009, 48:166-175. 10.1016/j.neuroimage.2009.05.026.
7. Bullmore E.T., Brammer M.J., Rabe-Hesketh S., Curtis V.A., Morris R.G., Williams S.C., Sharma T., McGuire P.K. Methods for diagnosis and treatment of stimulus-correlated motion in generic brain activation studies using fMRI. Hum. Brain Mapp. 1999, 7:38-48.
8. Chang C., Cunningham J.P., Glover G.H. Influence of heart rate on the BOLD signal: the cardiac response function. NeuroImage 2009, 44:857-869. 10.1016/j.neuroimage.2008.09.029.
9. Churchill N.W., Yourganov G., Oder A., Tam F., Graham S.J., Strother S.C. Optimizing preprocessing and analysis pipelines for single-subject fMRI: 2. Interactions with ICA, PCA, task contrast and inter-subject heterogeneity. PLoS ONE 2012, 7:e31147. 10.1371/journal.pone.0031147.
10. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
11. Di Martino A., Yan C.-G., Li Q., Denio E., Castellanos F.X., Alaerts K., Anderson J.S., Assaf M., Bookheimer S.Y., Dapretto M., Deen B., Delmonte S., Dinstein I., Ertl-Wagner B., Fair D.A., Gallagher L., Kennedy D.P., Keown C.L., Keysers C., Lainhart J.E., Lord C., Luna B., Menon V., Minshew N.J., Monk C.S., Mueller S., Müller R.-A., Nebel M.B., Nigg J.T., O'Hearn K., Pelphrey K.A., Peltier S.J., Rudie J.D., Sunaert S., Thioux M., Tyszka J.M., Uddin L.Q., Verhoeven J.S., Wenderoth N., Wiggins J.L., Mostofsky S.H., Milham M.P. The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol. Psychiatry 2013, 19:659-667. 10.1038/mp.2013.78.
12. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 1995, 33:636-647.
13. 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.
14. Glover G.H., Li T.Q., Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000, 44:162-167.
15. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. Neuroimage 2012, 62:782-790. 10.1016/j.neuroimage.2011.09.015.
16. Jo H.J., Saad Z.S., Simmons W.K., Milbury L.A., Cox R.W. Mapping sources of correlation in resting state FMRI, with artifact detection and removal. NeuroImage 2010, 52:571-582. 10.1016/j.neuroimage.2010.04.246.
17. Lund T.E., Madsen K.H., Sidaros K., Luo W.-L., Nichols T.E. Non-white noise in fMRI: does modelling have an impact?. NeuroImage 2006, 29:54-66. 10.1016/j.neuroimage.2005.07.005.
18. McKay L.C., Evans K.C., Frackowiak R.S.J., Corfield D.R. Neural correlates of voluntary breathing in humans. J. Appl. Physiol. 2003, 95:1170-1178. 10.1152/japplphysiol.00641.2002.
19. Moodie C.A., Wisner K.M., MacDonald A.W. Characteristics of canonical intrinsic connectivity networks across tasks and monozygotic twin pairs. Hum. Brain Mapp. 2014, 10.1002/hbm.22568.
20. Murphy K., Birn R.M., Bandettini P.A. Resting-state fMRI confounds and cleanup. NeuroImage 2013, 80:349-359. 10.1016/j.neuroimage.2013.04.001.
21. 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.
22. 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.
23. 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, 10.1016/j.neuroimage.2014.06.065.
24. 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.
25. 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.
26. Shmueli K., van Gelderen P., de Zwart J.A., Horovitz S.G., Fukunaga M., Jansma J.M., Duyn J.H. Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. NeuroImage 2007, 38:306-320. 10.1016/j.neuroimage.2007.07.037.
27. 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. 10.1073/pnas.0905267106.
28. Taylor P.A., Gohel S., Di X., Walter M., Biswal B.B. Functional covariance networks: obtaining resting-state networks from intersubject variability. Brain Connect. 2012, 2:203-217. 10.1089/brain.2012.0095.
29. Tie Y., Rigolo L., Norton I.H., Huang R.Y., Wu W., Orringer D., Mukundan S., Golby A.J. Defining language networks from resting-state fMRI for surgical planning-a feasibility study. Hum. Brain Mapp. 2014, 35:1018-1030. 10.1002/hbm.22231.
30. 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. 10.1152/jn.00783.2009.
31. 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. 10.1016/j.neuroimage.2011.07.044.
32. Wise R.G., Ide K., Poulin M.J., Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. NeuroImage 2004, 21:1652-1664. 10.1016/j.neuroimage.2003.11.025.
33. 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. 10.1016/j.neuroimage.2013.02.066.
34. 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.
35. Yan C.-G., Craddock R.C., He Y., Milham M.P. Addressing head motion dependencies for small-world topologies in functional connectomics. Front. Hum. Neurosci. 2013, 7. 10.3389/fnhum.2013.00910.
36. 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 2014, 111:6058-6062. 10.1073/pnas.1317424111.
37. Zhu S., Fang Z., Hu S., Wang Z., Rao H. Resting state brain function analysis using concurrent BOLD in ASL perfusion fMRI. PLoS ONE 2013, 8:e65884. 10.1371/journal.pone.0065884.