Integrated strategy for improving functional connectivity mapping using multiecho fMRI
Open accessAbstract
Functional connectivity analysis of resting state blood oxygen level–dependent (BOLD) functional MRI is widely used for noninvasively studying brain functional networks. Recent findings have indicated, however, that even small (≤1 mm) amounts of head movement during scanning can disproportionately bias connectivity estimates, despite various preprocessing efforts. Further complications for interregional connectivity estimation from time domain signals include the unaccounted reduction in BOLD degrees of freedom related to sensitivity losses from high subject motion. To address these issues, we describe an integrated strategy for data acquisition, denoising, and connectivity estimation. This strategy builds on our previously published technique combining data acquisition with multiecho (ME) echo planar imaging and analysis with spatial independent component analysis (ICA), called ME-ICA, which distinguishes BOLD (neuronal) and non-BOLD (artifactual) components based on linear echo-time dependence of signals—a characteristic property of BOLD signal changes. Here we show for 32 control subjects that this method provides a physically principled and nearly operator-independent way of removing complex artifacts such as motion from resting state data. We then describe a robust estimator of functional connectivity based on interregional correlation of BOLD-independent component coefficients. This estimator, called independent components regression, considerably simplifies statistical inference for functional connectivity because degrees of freedom equals the number of independent coefficients. Compared with traditional connectivity estimation methods, the proposed strategy results in fourfold improvements in signal-to-noise ratio, functional connectivity analysis with improved specificity, and valid statistical inference with nominal control of type 1 error in contrasts of connectivity between groups with different levels of subject motion.
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Multi-echo EPI acquisition and the ME-ICA denoising technique greatly enhance temporal signal-to-noise ratio and allow for enhanced ability to reduce false positives.
“Multi-echo EPI acquisition and the ME-ICA denoising technique employed here is known to greatly enhance temporal signal-to-noise ratio and allow for enhanced ability to reduce false positives.31”
From Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women (2017) · cites this paper as [31]
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Cites
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
Functional connectivity in the motor cortex of resting human brain using echo‐planar mri
Biswal, B., Zerrin Yetkin, F., Haughton, V. M., & Hyde, J. S. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910340409 · Cited by 9,812 · see citing works
Independent component analysis: algorithms and applications
Hyvärinen, A., & Erkki Oja, A. (2000) · Neural Networks · doi:10.1016/s0893-6080(00)00026-5 · Cited by 8,726 · see citing works
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.018 · Cited by 7,429 · see citing works
Probabilistic Independent Component Analysis for Functional Magnetic Resonance Imaging
Beckmann, C. F., & Smith, S. M. (2004) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2003.822821 · Cited by 2,707 · see citing works
Analysis of fMRI Time-Series Revisited
Friston, K. J., Holmes, A. P., Poline, J., Grasby, P. M., Williams, S., Frackowiak, R. S. J., & Turner, R. (1995) · NeuroImage · doi:10.1006/nimg.1995.1007 · Cited by 2,504 · see citing works
Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.09.036 · Cited by 2,387 · see citing works
Self-citationThe influence of head motion on intrinsic functional connectivity MRI
Van Dijk, K. R. A., Sabuncu, M. R., & Buckner, R. L. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.044 · Cited by 2,344 · see citing works
Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration
Klein, A., Andersson, J., Ardekani, B. A., Ashburner, J., Avants, B., Chiang, M.-C., Christensen, G. E., Collins, D. L., Gee, J., Hellier, P., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.12.037 · Cited by 2,227 · see citing works
The Intraclass Correlation Coefficient as a Measure of Reliability
Bartko, J. (1966) · Psychological Reports · doi:10.2466/pr0.1966.19.1.3 · Cited by 2,206 · see citing works
Satterthwaite, T., Elliott, M., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M., Eickhoff, S., Hakonarson, H., Gur, R., Gur, R. E., et al. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.08.052 · Cited by 1,900 · see citing works
Distinct patterns of brain activity in young carriers of the <i>APOE</i> -ε4 allele
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. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811879106 · Cited by 1,613 · see citing works
Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging
Feinberg, D. A., Moeller, S., Smith, S. M., Auerbach, E., Ramanna, S., Glasser, M. F., Miller, K. L., Ugurbil, K., & Yacoub, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015710 · Cited by 1,296 · see citing works
Setsompop, K., Gagoski, B. A., Polimeni, J. R., Witzel, T., Wedeen, V. J., & Wald, L. L. (2012) · Magnetic Resonance in Medicine · doi:10.1002/mrm.23097 · Cited by 1,285 · see citing works
Satterthwaite, T. D., Wolf, D. H., Loughead, J., Ruparel, K., Elliott, M. A., Hakonarson, H., Gur, R. C., & Gur, R. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.063 · Cited by 1,125 · see citing works
Bullmore, E. T., Suckling, J., Overmeyer, S., Rabe-Hesketh, S., Taylor, E., & Brammer, M. J. (1999) · IEEE Transactions on Medical Imaging · doi:10.1109/42.750253 · Cited by 1,088 · see citing works
Self-citationSaad, Z. S., Gotts, S. J., Murphy, K., Chen, G., Jo, H. J., Martin, A., & Cox, R. W. (2012) · Brain Connectivity · doi:10.1089/brain.2012.0080 · Cited by 859 · see citing works
Self-citationTemporally-independent functional modes of spontaneous brain activity
Smith, S. M., Miller, K. L., Moeller, S., Xu, J., Auerbach, E. J., Woolrich, M. W., Beckmann, C. F., Jenkinson, M., Andersson, J., Glasser, M. F., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121329109 · Cited by 702 · see citing works
Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI
Kundu, P., Inati, S., Evans, J. W., Luh, W., & Bandettini, P. A. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.028 · Cited by 604 · see citing works
Self-citationPoser, B. A., Versluis, M. J., Hoogduin, J. M., & Norris, D. G. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20900 · Cited by 440 · see citing works
A simple view of the brain through a frequency-specific functional connectivity measure
Salvador, R., Martínez, A., Pomarol-Clotet, E., Gomar, J., Vila, F., Sarró, S., Capdevila, A., & Bullmore, E. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.08.018 · Cited by 225 · see citing works
Self-citationT2* Dependence of Low Frequency Functional Connectivity
Peltier, S. J. (2002) · NeuroImage · doi:10.1006/nimg.2002.1141 · Cited by 102 · see citing works
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Ciric, R., Wolf, D. H., Power, J. D., Roalf, D. R., Baum, G. L., Ruparel, K., Shinohara, R. T., Elliott, M. A., Eickhoff, S. B., Davatzikos, C., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.020 · Cited by 1,042 · see citing works
Recent progress and outstanding issues in motion correction in resting state fMRI
Power, J. D., Schlaggar, B. L., & Petersen, S. E. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.044 · Cited by 957 · see citing works
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Caballero-Gaudes, C., & Reynolds, R. C. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.12.018 · Cited by 542 · see citing works
Vaghi, M. M., Vértes, P. E., Kitzbichler, M. G., Apergis-Schoute, A. M., van der Flier, F. E., Fineberg, N. A., Sule, A., Zaman, R., Voon, V., Kundu, P., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.009 · Cited by 290 · see citing works
Self-citationPassamonti, L., Tsvetanov, K. A., Jones, P. S., Bevan-Jones, W. R., Arnold, R., Borchert, R. J., Mak, E., Su, L., O'Brien, J. T., & Rowe, J. B. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2574-18.2019 · Cited by 220 · see citing works
Alexander-Bloch, A., Clasen, L., Stockman, M., Ronan, L., Lalonde, F., Giedd, J., & Raznahan, A. (2016) · Human Brain Mapping · doi:10.1002/hbm.23180 · Cited by 178 · see citing works
Morris, L. S., Kundu, P., Dowell, N., Mechelmans, D. J., Favre, P., Irvine, M. A., Robbins, T. W., Daw, N., Bullmore, E. T., Harrison, N. A., et al. (2016) · Cortex · doi:10.1016/j.cortex.2015.11.004 · Cited by 198 · see citing works
Self-citationVértes, P. E., & Bullmore, E. T. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12365 · Cited by 197 · see citing works
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Advanced MRI techniques to improve our understanding of experience-induced neuroplasticity
Tardif, C. L., Gauthier, C. J., Steele, C. J., Bazin, P.-L., Schäfer, A., Schaefer, A., Turner, R., & Villringer, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2015.08.047 · Cited by 127 · see citing works
Motion artifact in studies of functional connectivity: Characteristics and mitigation strategies
Satterthwaite, T. D., Ciric, R., Roalf, D. R., Davatzikos, C., Bassett, D. S., & Wolf, D. H. (2019) · Human Brain Mapping · doi:10.1002/hbm.23665 · Cited by 137 · see citing works
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Morris, L. S., Costi, S., Tan, A., Stern, E. R., Charney, D. S., & Murrough, J. W. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-019-0591-5 · Cited by 104 · see citing works
Customized head molds reduce motion during resting state fMRI scans
Power, J. D., Silver, B. M., Silverman, M. R., Ajodan, E. L., Bos, D. J., & Jones, R. M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.01.016 · Cited by 88 · see citing works
Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women
Bethlehem, R. A. I., Lombardo, M. V., Lai, M.-C., Auyeung, B., Crockford, S. K., Deakin, J., Soubramanian, S., Sule, A., Kundu, P., Voon, V, et al. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.72 · Cited by 96 · see citing works
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Costi, S., Morris, L. S., Collins, A., Fernandez, N. F., Patel, M., Xie, H., Kim-Schulze, S., Stern, E. R., Collins, K. A., Cathomas, F., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01668-1 · Cited by 87 · see citing works
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DiNuzzo, M., Mascali, D., Moraschi, M., Bussu, G., Maugeri, L., Mangini, F., Fratini, M., & Giove, F. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00965 · Cited by 74 · see citing works
Moeller, S. J., Kundu, P., Bachi, K., Maloney, T., Malaker, P., Parvaz, M. A., Alia-Klein, N., London, E. D., & Goldstein, R. Z. (2020) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2020.107930 · Cited by 14 · see citing works
Self-citationChowdhury, A., Boukezzi, S., Costi, S., Hameed, S., Jacob, Y., Salas, R., Iosifescu, D. V., Han, M.-H., Swann, A., Mathew, S. J., et al. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.02.897 · Cited by 10 · see citing works
Hart, M. G., Romero-Garcia, R., Price, S. J., Santarius, T., & Suckling, J. (2020) · World Neurosurgery · doi:10.1016/j.wneu.2020.03.116 · Cited by 7 · see citing works
- Authors
- Kundu, P., Brenowitz, N. D., Voon, V., Worbe, Y., Vértes, P. E., Inati, S. J., Saad, Z. S., Bandettini, P. A., & Bullmore, E. T.
- Affiliations
- University of Cambridge (GB)
- Section on Functional Imaging Methods,
- Functional MRI Core Facility, and
- National Institute of Mental Health (US)
- GlaxoSmithKline (United Kingdom) (GB)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-09-13
- Volume
- 110
- Issue
- 40
- Pages
- 16187-16192
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3791700
- OpenAlex
- W2041127567
- Cited by
- 399
- References
- 22
- Citations by year
- 2026: 34 · 2025: 44 · 2024: 38 · 2023: 22 · 2022: 44 · 2021: 50 · 2020: 29 · 2019: 31 · 2018: 24 · 2017: 23 · 2016: 29 · 2015: 16 · 2014: 15
- FWCI
- 10.97
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- functional connectivity, resting-state fMRI, motion artifact removal, BOLD signal, spatial independent component analysis, degrees of freedom, signal-to-noise ratio, type I error control, functional brain networks
- MeSH terms
- Brain Mapping, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Neural Pathways, Oxygen, Research Design, Sensitivity and Specificity, Artifacts, Signal-To-Noise Ratio
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