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A practical model-based segmentation approach for improved activation detection in single-subject functional Magnetic Resonance Imaging studies (2102.03639v3)

Published 6 Feb 2021 in stat.AP, stat.CO, stat.ME, and stat.ML

Abstract: Functional Magnetic Resonance Imaging (fMRI) maps cerebral activation in response to stimuli but this activation is often difficult to detect, especially in low-signal contexts and single-subject studies. Accurate activation detection can be guided by the fact that very few voxels are, in reality, truly activated and that these voxels are spatially localized, but it is challenging to incorporate both these facts. We address these twin challenges to single-subject and low-signal fMRI by developing a computationally feasible and methodologically sound model-based approach, implemented in the R package MixfMRI, that bounds the a priori expected proportion of activated voxels while also incorporating spatial context. An added benefit of our methodology is the ability to distinguish voxels and regions having different intensities of activation. Our suggested approach is evaluated in realistic two- and three-dimensional simulation experiments as well as on multiple real-world datasets. Finally, the value of our suggested approach in low-signal and single-subject fMRI studies is illustrated on a sports imagination experiment that is often used to detect awareness and improve treatment in patients in persistent vegetative state (PVS). Our ability to reliably distinguish activation in this experiment potentially opens the door to the adoption of fMRI as a clinical tool for the improved treatment and therapy of PVS survivors and other patients.

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References (91)
  1. J. W. Belliveau, D. N. Kennedy, R. C. McKinstry, B. R. Buchbinder, R. M. Weisskoff, M. S. Cohen, J. M. Vevea, T. J. Brady, and B. R. Rosen, “Functional mapping of the human visual cortex by magnetic resonance imaging,” Science, vol. 254, pp. 716–719, 1991.
  2. K. K. Kwong, J. W. Belliveau, D. A. Chesler, I. E. Goldberg, R. M. Weisskoff, B. P. Poncelet, D. N. Kennedy, B. E. Hoppel, M. S. Cohen, R. Turner, H.-M. Cheng, T. J. Brady, and B. R. Rosen, “Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation,” Proceedings of the National Academy of Sciences, vol. 89, pp. 5675–5679, 1992.
  3. P. A. Bandettini, A. Jesmanowicz, E. C. Wong, and J. S. Hyde, “Processing strategies for time-course data sets in functional MRI of the human brain,” Magnetic Resonance in Medicine, vol. 30, pp. 161–173, 1993.
  4. A. M. Howseman and R. W. Bowtell, “Functional magnetic resonance imaging: imaging techniques and contrast mechanisms,” Philosophical Transactional of the Royal Society, London, vol. 354, pp. 1179–94, 1999.
  5. M. A. Lindquist, “The statistical analysis of fMRI data,” Statistical Science, vol. 23, no. 4, pp. 439–464, 2008.
  6. S. Ogawa, T. M. Lee, A. S. Nayak, and P. Glynn, “Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields,” Magnetic Resonance in Medicine, vol. 14, pp. 68–78, 1990.
  7. S. Ogawa, T. M. Lee, A. R. Kay, and D. W. Tank, “Brain magnetic resonance imaging with contrast dependent on blood oxygenation,” Proceedings of the National Academy of Sciences, vol. 87, no. 24, pp. 9868–9872, 1990.
  8. K. J. Friston, A. P. Holmes, K. J. Worsley, J.-B. Poline, C. D. Frith, and R. S. J. Frackowiak, “Statistical parametric maps in functional imaging: A general linear approach,” Human Brain Mapping, vol. 2, pp. 189–210, 1995.
  9. K. J. Friston, C. D. Frith, P. F. Liddle, R. J. Dolan, A. A. Lammertsma, and R. S. J. Frackowiak, “The relationship between global and local changes in PET scans,” Journal of Cerebral Blood Flow and Metabolism, vol. 10, pp. 458–466, 1990.
  10. K. J. Worsley, S. Marrett, P. Neelin, A. C. Vandal, K. J. Friston, and A. C. Evans, “A unified statistical approach for determining significant voxels in images of cerebral activation,” Human Brain Mapping, vol. 4, pp. 58–73, 1996.
  11. C. R. Genovese, N. A. Lazar, and T. Nichols, “Thresholding of statistical maps in functional neuroimaging using the false discovery rate,” Neuroimage, vol. 15, pp. 870–878, 2002.
  12. B. R. Logan and D. B. Rowe, “An evaluation of thresholding techniques in fMRI analysis,” NeuroImage, vol. 22, pp. 95–108, 2004.
  13. M. M. Monti, “Statistical analysis of fMRI time-series: A critical review of the GLM approach,” Frontiers in Human Neuroscience, vol. 5, no. 00028, pp. 1–13, 2011. [Online]. Available: http://www.frontiersin.org/Journal/Abstract.aspx?s=537&name=human_neuroscience&ART_DOI=10.3389/fnhum.2011.00028
  14. B. Biswal, A. E. DeYoe, and J. S. Hyde, “Reduction of physiological fluctuations in fMRI using digital filters.” Magnetic Resonance in Medicine, vol. 35, no. 1, pp. 107–113, January 1996. [Online]. Available: http://view.ncbi.nlm.nih.gov/pubmed/8771028
  15. J. V. Hajnal, R. Myers, A. Oatridge, J. E. Schweiso, J. R. Young, and G. M. Bydder, “Artifacts due to stimulus-correlated motion in functional imaging of the brain,” Magnetic Resonance in Medicine, vol. 31, pp. 283–291, 1994.
  16. R. Maitra, S. R. Roys, and R. P. Gullapalli, “Test-retest reliability estimation of functional MRI data,” Magnetic Resonance in Medicine, vol. 48, pp. 62–70, 2002.
  17. R. P. Gullapalli, R. Maitra, S. Roys, G. Smith, G. Alon, and J. Greenspan, “Reliability estimation of grouped functional imaging data using penalized maximum likelihood,” Magnetic Resonance in Medicine, vol. 53, pp. 1126–1134, 2005.
  18. R. Maitra, “Assessing certainty of activation or inactivation in test-retest fMRI studies,” Neuroimage, vol. 47, pp. 88–97, 2009.
  19. T. E. Nichols and S. Hayasaka, “Controlling the familywise error rate in functional neuroimaging: a comparative review,” Statistical Methods in Medical Research, vol. 12, pp. 419–446, 2003.
  20. Y. Benjamini and R. Heller, “False discovery rates for spatial signals,” Journal of the American Statistical Association, vol. 102, no. 480, pp. 1272–1281, 2007.
  21. ——, “Screening for partial conjunction hypotheses,” Biometrics, vol. 64, pp. 1215–1222, 2008.
  22. K. J. Friston, C. Frith, P. Liddle, and R. Frackowiak, “Comparing functional (pet) images: the assessment of significant change,” Journal of Cerebral Blood Flow and Metabolism, vol. 11, no. 4, p. 690, 1991.
  23. K. J. Worsley, A. C. Evans, S. Marrett, and P. Neelin, “A three-dimensional statistical analysis for CBF activation studies in human brain,” Journal of Cerebral Blood Flow and Metabolism, vol. 12, no. 6, p. 900–918, 1992.
  24. K. J. Worsley, “Local maxima and the expected Euler characteristic of excursion sets of χ2superscript𝜒2\chi^{2}italic_χ start_POSTSUPERSCRIPT 2 end_POSTSUPERSCRIPT, F𝐹{F}italic_F and t𝑡titalic_t fields,” Advances in Applied Probability, vol. 26, pp. 13–42, 1994.
  25. K. J. Worsley and J. E. Taylor, “An improved theoretical p𝑝pitalic_p value for SPMs based on discrete local maxima,” NeuroImage, vol. 28, p. 1056–1062, 2005.
  26. K. J. Friston, P. Jezzard, and R. Turner, “Analysis of functional MRI time-series,” Human Brain Mapping, vol. 1, pp. 153–171, 1994.
  27. S. Hayasaka and T. E. Nichols, “Validating cluster size inference: random field and permutation methods,” Neuroimage, vol. 20, p. 2343–2356, 2003.
  28. S. Forman, J. Cohen, M. Fitzgerald, W. Eddy, M. Mintun, and D. Noll, “Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold,” Magnetic Resonance in Medicine, vol. 33, p. 636–647, 1995.
  29. C.-W. Woo, A. Krishnan, and T. D. Wager, “Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations,” Neuroimage, vol. 91, p. 412–419, 2014.
  30. S. M. Smith and T. E. Nichols, “Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference,” Neuroimage, vol. 44, pp. 83–98, 2009.
  31. R. Heller, D. Stanley, D. Yekutieli, N. Rubin, and Y. Benjamini, “Cluster-based analysis of fMRI data,” NeuroImage, vol. 33, no. 2, pp. 599–608, Nov. 2006. [Online]. Available: http://dx.doi.org/10.1016/j.neuroimage.2006.04.233
  32. T. Spisák, Z. Spisák, M. Zunhammer, U. Bingel, S. Smith, T. Nichols, and T. Kincses, “Probabilistic TFCE: A generalized combination of cluster size and voxel intensity to increase statistical power,” NeuroImage, vol. 185, pp. 12 – 26, 2019.
  33. A. Eklund, T. Nichols, M. Andersson, and H. Knutsson, “Empirically investigating the statistical validity of SPM, FSL and AFNI for single subject fMRI analysis,” in IEEE International symposium on biomedical imaging (ISBI), 2015, p. 1376–1380.
  34. D. Kessler, M. Angstadt, and C. S. Sripada, “Reevaluating ”cluster failure” in fMRI using nonparametric control of the false discovery rate,” Proceedings of the National Academy of Sciences, vol. 114, no. 17, pp. E3372–E3373, 2017. [Online]. Available: http://www.pnas.org/content/114/17/E3372
  35. R. W. Cox, G. Chen, D. R. Glen, R. C. Reynolds, and P. A. Taylor, “fMRI clustering and false-positive rates,” Proceedings of the National Academy of Sciences, vol. 114, no. 17, pp. E3370–E3371, 2017. [Online]. Available: http://www.pnas.org/content/114/17/E3370
  36. Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Working Group Report to the Advisory Committee to the Director, NIH, “BRAIN 2025: A SCIENTIFIC VISION,” 2014.
  37. E. N. Brown and M. Behrmann, “Controversy in statistical analysis of functional magnetic resonance imaging data,” Proceedings of the National Academy of Sciences, vol. 114, no. 17, pp. E3368–E3369, 2017. [Online]. Available: http://www.pnas.org/content/114/17/E3368
  38. I. A. Almodóvar-Rivera and R. Maitra, “FAST adaptive smoothed thresholding for improved activation detection in low-signal fMRI,” IEEE Transactions on Medical Imaging, vol. 38, no. 12, pp. 2821–2828, 2019.
  39. N. V. Hartvig and J. L. Jensen, “Spatial mixture modeling of fMRI data,” Human Brain Mapping, vol. 11, no. 4, pp. 233–248, 2000. [Online]. Available: http://dx.doi.org/10.1002/1097-0193(200012)11:4<233::AID-HBM10>3.0.CO;2-F
  40. C. R. Genovese, “A Bayesian time-course model for functional Magnetic Resonance Imaging data (with discussion),” Journal of the American Statistical Association, vol. 95, no. 451, pp. 691–719, 2000.
  41. M. Smith and L. Fahrmeir, “Spatial bayesian variable selection with application to functional magnetic resonance imaging,” Journal of the American Statistical Association, vol. 102, no. 478, pp. 417–431, 2007. [Online]. Available: http://pubs.amstat.org/doi/abs/10.1198/016214506000001031
  42. K. Friston, W. Penny, C. Phillips, S. Kiebel, G. Hinton, and J. Ashburner, “Classical and bayesian inference in neuroimaging: Theory,” NeuroImage, vol. 16, no. 2, pp. 465–483, 2002. [Online]. Available: https://www.sciencedirect.com/science/article/pii/S1053811902910906
  43. K. Friston, D. Glaser, R. Henson, S. Kiebel, C. Phillips, and J. Ashburner, “Classical and bayesian inference in neuroimaging: Applications,” NeuroImage, vol. 16, no. 2, pp. 484–512, 2002. [Online]. Available: https://www.sciencedirect.com/science/article/pii/S1053811902910918
  44. F. D. Bowman, B. Caffo, S. S. Bassett, and C. Kilts, “A bayesian hierarchical framework for spatial modeling of fmri data,” NeuroImage, vol. 39, no. 1, pp. 146–156, 2008. [Online]. Available: https://www.sciencedirect.com/science/article/pii/S1053811907007306
  45. W.-Y. Ahn, A. Krawitz, W. Kim, J. R. Busemeyer, and J. W. Brown, “A model-based fmri analysis with hierarchical bayesian parameter estimation,” Journal of Neuroscience, Psychology, and Economics, vol. 4, no. 2, p. 95–110, 2011.
  46. The Multi-Society Task Force on PVS, “Medical aspects of the persistent vegetative state,” New England Journal of Medicine, vol. 330, pp. 1499–1508, 1994.
  47. N. D. Schiff, U. Ribary, D. R. Moreno, B. Beattie, E. Kronberg, R. Blasberg, J. Giacino, C. McCagg, J. J. Fins, R. Llinás, and F. Plum, “Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain,” Brain, vol. 125, no. 6, pp. 1210–1234, 2002.
  48. A. M. Owen, M. R. Coleman, M. Boly, M. H. Davis, S. Laureys, and J. D. Pickard, “Detecting awareness in the vegetative state,” Science, vol. 313, no. 5792, p. 1402, 2006.
  49. M. M. Monti, A. Vanhaudenhuyse, M. R. Coleman, M. Boly, J. D. Pickard, L. Tshibanda, A. M. Owen, and S. Laureys, “Willful modulation of brain activity in disorders of consciousness,” New England Journal of Medicine, vol. 362, no. 7, p. 579–89, 2010.
  50. J. C. Bardin, J. J. Fins, D. I. Katz, J. Hersh, L. A. Heier, K. Tabelow, J. P. Dyke, D. J. Ballon, N. D. Schiff, and H. U. Voss, “Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury,” Brain, vol. 134, pp. 769–782, 2011.
  51. K. Tabelow and J. Polzehl, “Statistical parametric maps for functional MRI experiments in R: The package fmri,” Journal of Statistical Software, vol. 44, no. 11, pp. 1–21, 10 2011. [Online]. Available: http://www.jstatsoft.org/v44/i11
  52. Y. Benjamini and D. Yekutieli, “The control of the false discovery rate in multiple testing under dependency,” The Annals of Statistics, vol. 29, no. 4, pp. 1165–1188, 2001. [Online]. Available: http://www.jstor.org/stable/2674075
  53. A. M. Winkler, G. R. Ridgway, M. A. Webster, S. M. Smith, and T. E. Nichols, “Permutation inference for the general linear model,” Neuroimage, vol. 92, pp. 381–397, 2014.
  54. R. W. Cox, “AFNI: software for analysis and visualization of functional magnetic resonance neuroimages,” Computers and biomedical research, an international journal, vol. 29, no. 3, pp. 162–173, 1996.
  55. R. W. Cox and J. S. Hyde, “Software tools for analysis and visualization of fMRI data,” NMR in Biomedicine, vol. 10, no. 4-5, pp. 171–178, 1997.
  56. R. W. Cox, “AFNI: What a long strange trip it has been,” NeuroImage, vol. 62, pp. 743–747, 2012.
  57. R. A. Parker and R. B. Rothenberg, “Identifying important results from multiple statistical tests,” Statistics in Medicine, vol. 7, pp. 1031–1043, 1988.
  58. D. B. Allison, G. L. Gadbury, M. Heo, J. R. Fernández, C.-K. Les, J. A. Prolla, and R. Weindruch, “A mixture model approach for the analysis of microarray gene expression data,” Computational Statistics and Data Analysis, vol. 39, pp. 1–20, 2002.
  59. S. Pounds and S. W. Morris, “Estimating the occurrence of false positives and false negatives in microarray studies by approximating and partitioning the empirical distribution of p𝑝pitalic_p-values,” Bioninformatics, vol. 19, pp. 1236–1242, 2003.
  60. A. P. Dempster, N. M. Laird, and D. B. Rubin, “Maximum likelihood for incomplete data via the EM algorithm (with discussion),” Jounal of the Royal Statistical Society, Series B, vol. 39, pp. 1–38, 1977.
  61. C. Wu, “On the convergence properties of the EM algorithm,” Annals of Statistics, vol. 11, pp. 95–103, 1983.
  62. X. Meng and D. van Dyk, “The EM algorithm — an old folk-song sung to a fast new tune (with discussion),” Journal of the Royal Statistical Society B, vol. 59, pp. 511–567, 1997.
  63. W.-C. Chen and R. Maitra, “Model-based clustering of regression time series data via APECM -— an AECM algorithm sung to an even faster beat,” Statistical Analysis and Data Mining, vol. 4, no. 6, pp. 567–578, 2011. [Online]. Available: http://dx.doi.org/10.1002/sam.10143
  64. W.-C. Chen, G. Ostrouchov, D. Pugmire, M. Prabhat, and M. Wehner, “A parallel em algorithm for model-based clustering with application to explore large spatio-temporal data,” Technometrics, vol. 55, pp. 513–523, 2013.
  65. R. Maitra, “Initializing partition-optimization algorithms,” IEEE/ACM Transactions on Computational Biology and Bioinformatics, vol. 6, pp. 144–157, 2009.
  66. R. Maitra and V. Melnykov, “Simulating data to study performance of finite mixture modeling and clustering algorithms,” Journal of Computational and Graphical Statistics, vol. 19, no. 2, pp. 354–376, 2010.
  67. V. Melnykov and R. Maitra, “Finite mixture models and model-based clustering,” Statistics Surveys, vol. 4, pp. 80–116, 2010.
  68. H. Akaike, “Information theory and an extension of the maximum likelihood principle,” in Selected Papers of Hirotugu Akaike.   Springer, 1973, pp. 199–213.
  69. G. Schwarz, “Estimating the dimensions of a model,” Annals of Statistics, vol. 6, pp. 461–464, 1978.
  70. R. E. Kass and A. E. Raftery, “Bayes factors,” Journal of the American Statistical Association, vol. 90, no. 430, pp. 773–795, 1995.
  71. Y. Benjamini and Y. Hochberg, “Controlling the false discovery rate: A practical and powerful approach to multiple testing,” Journal of the Royal Statistical Society. Series B (Methodological), vol. 57, no. 1, pp. 289–300, 1995. [Online]. Available: http://dx.doi.org/10.2307/2346101
  72. J. Polzehl, H. U. Voss, and K. Tabelow, “Structural adaptive segmentation for statistical parametric mapping,” NeuroImage, vol. 52, no. 2, pp. 515–523, 2010.
  73. W.-C. Chen and R. Maitra, “MixfMRI: fMRI clustering analysis,” 2017, r Package, http://cran.r-project.org/package=MixfMRI.
  74. C. Bordier, M. Dojat, and P. L. de Micheaux, “Temporal and spatial independent component analysis for fMRI data sets embedded in the AnalyzeFMRI R package,” Journal of Statistical Software, vol. 44, no. 9, pp. 1–24, 2011. [Online]. Available: http://www.jstatsoft.org/v44/i09/
  75. P. Jaccard, “Ètude comparative de la distribution florale dans une portion des alpes et des jura,” Bulletin del la Sociètè Vaudoise des Sciences Naturelles, vol. 37, p. 547–579, 1901.
  76. R. Maitra, “A re-defined and generalized percent-overlap-of-activation measure for studies of fMRI reproducibility and its use in identifying outlier activation maps,” Neuroimage, vol. 50, pp. 124–135, 2010.
  77. L. Hubert and P. Arabie, “Comparing partitions,” Journal of classification, vol. 2, no. 1, pp. 193–218, 1985.
  78. Y. Vardi, L. A. Shepp, and L. A. Kaufman, “Statistical model for Positron Emission Tomography,” Journal of the American Statistical Association, vol. 80, pp. 8–37, 1985.
  79. R. Maitra and F. O’Sullivan, “Variability assessment in Positron Emission Tomography and related generalized deconvolution models,” Journal of the American Statistical Association, vol. 93, pp. 1340–1355, 1998.
  80. M. Welvaert, J. Durnez, B. Moerkerke, G. Verdoolaege, and Y. Rosseel, “neuRosim: An R package for generating fMRI data,” Journal of Statistical Software, vol. 44, no. 10, pp. 1–18, 2011. [Online]. Available: http://www.jstatsoft.org/v44/i10/
  81. R. Henson, T. Shallice, M. Gorno-Tempini, and R. Dolan, “Face Repetition Effects in Implicit and Explicit Memory Tests as Measured by fMRI,” Cerebral Cortex, vol. 12, no. 2, pp. 178–186, 02 2002.
  82. M. B. Nebel, S. Joel, J. Muschelli, A. Barber, B. Caffo, J. Pekar, and S. Mostofsky, “Disruption of functional organization within the primary motor cortex in children with autism,” Human Brain Mapping, vol. 35, pp. 567–580, 02 2014.
  83. A. C. Kelly, L. Q. Uddin, B. B. Biswal, F. X. Castellanos, and M. P. Milham, “Competition between functional brain networks mediates behavioral variability,” NeuroImage, vol. 39, no. 1, pp. 527–537, 2008.
  84. D. Garcia, “Robust smoothing of gridded data in one and higher dimensions with missing values,” Computational Statistics and Data Analysis, vol. 54, pp. 1167–1178, 2010.
  85. M. Roth, J. Decety, M. Raybaudi, R. Massarelli, C. Delon-Martin, C. Segabarth, S. Morand, A. Gemignani, M. Decorps, and M. Jeannerod, “Possible involvement of primary motor cortex in mentally stimulated movement: a functional magnetic resonance imaging study,” NeuroReport, vol. 7, p. 1280–1284, 1996.
  86. M. Lotze, P. Montoya, M. Erb, E. Hülsmann, H. Flor, U. Klose, N. Birbaumer, and W. Grodd, “Activation of cortical and cerebellar motor areas during executed and imaginated hand movements: a functional MRI study,” Journal of Cognitive Neuroscience, vol. 11, p. 491–501, 1999.
  87. C. Stippich, H. Ochmann, and K. Sartor, “Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging,” Neuroscience Letters, vol. 331, p. 50–54, 2002.
  88. D. W. Adrian, R. Maitra, and D. B. Rowe, “Complex-valued time series modeling for improved activation detection in fMRI studies,” Annals of Applied Statistics, vol. 12, no. 3, pp. 1451–1478, 2018.
  89. R. W. Cox and A. Jesmanowicz, “Real-time 3d image registration for function MRI,” Magnetic Resonance in Medicine, vol. 42, pp. 1014–1018, 1999.
  90. Z. S. Saad, D. R. Glen, G. Chen, M. S. Beauchamp, R. Desai, and R. W. Cox, “A new method for improving functional-to-structural mri alignment using local pearson correlation,” NeuroImage, vol. 44, pp. 839–848, 2009.
  91. Z. S. Saad and R. C. Reynolds, “SUMA,” NeuroImage, vol. 62, pp. 767–772, 2012.

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