Interplay between functional connectivity and scale-free dynamics in intrinsic fMRI networks

NeuroImage

Volumn 95, Issue , 2014, Pages 248-263

  Ciuciu, Philippe ^a   Abry, Patrice ^b   He, Biyu J ^c  

^a DIF   (France)

^b UNIVERSITÉ DE LYON   (France)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Cross temporal dynamics; FMRI; Intrinsic brain activity; Scale free dynamics; Task modulation

Indexed keywords

ADULT; ARTICLE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; RESPONSE TIME; RESTING STATE NETWORK; TASK PERFORMANCE; VISUAL MEMORY; ADOLESCENT; BRAIN; BRAIN MAPPING; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; THEORETICAL MODEL; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MODELS, THEORETICAL; NEURAL PATHWAYS; YOUNG ADULT;

EID: 84900546045     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.047     Document Type: Article

References (93)

1. Abry P., Veitch D. Wavelet analysis of long-range-dependent traffic. IEEE Trans. Inf. Theory 1998, 44:2-15.
2. Abry P., Gonçalvès P., Flandrin P. Wavelets, Spectrum Estimation and 1/f Processes 1995, Springer-Verlag, New York, (Ch. 103, wavelets and Statistics, Lecture Notes in Statistics).
3. Abry P., Baraniuk R., Flandrin P., Riedi R., Veitch D. Multiscale network traffic analysis, modeling, and inference using wavelets, multifractals, and cascades. IEEE Signal Proc. Mag. 2002, 3(19):28-46.
4. Achard S., Salvador R., Whitcher B., Suckling J., Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 2006, 26(1):63-72.
5. Allen E.A., Damaraju E., Plis S.M., Erhardt E.B., Eichele T., Calhoun V.D. Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 2014 Mar, 24(3):663-676. Epub 2012 Nov 11. 10.1093/cercor/bhs352.
6. Amblard P., Coeurjolly J.-F. Identification of the multivariate fractional Brownian motion. IEEE Trans. Sign. Process. 2011, 59(11):5152-5168.
7. 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. 2005, 3601457:1001-1013.
8. Beran J. Statistics for Long-Memory Processes 1994, Chapman and Hall/CRC, Boca Raton, FL, USA.
9. Biswal B., Zerrin Yetkin F., Haughton V., Hyde J. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34(4):537-541.
10. Boyacioǧlu R., Barth M. Generalized iNverse imaging (GIN): ultrafast fMRI with physiological noise correction. Magn. Reson. Med. 2012, 1-10. (URL http://www.ncbi.nlm.nih.gov/pubmed/23097342).
11. Bullmore E., Long C., Suckling J., Fadili J., Calvert G., Zelaya F., Carpenter T., Brammer M. Colored noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum. Brain Mapp. 2001, 12(2):61-78.
12. Calhoun V.D., Adali T., Pearlson G.D., Pekar J. A method for making group inferences from functional MRI data using independent component analysis. Hum. Brain Mapp. 2001, 143:140-151.
13. Chang C., Glover G.H. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. NeuroImage 2010, 501:81-98.
14. Chen Z., Ivanov P., Hu K., Stanley H. Effect of nonstationarities on detrended fluctuation analysis. Physical Review E 2002, 65. (4 (Pt1)).
15. Ciuciu P., Abry P., Rabrait C., Wendt H. Log wavelet leaders cumulant based multifractal analysis of EVI fMRI time series: evidence of scaling in ongoing and evoked brain activity. IEEE J. Sel. Top. Sign. Process. 2008, 2(6):929-943.
16. Ciuciu P., Varoquaux G., Abry P., Sadaghiani S., Kleinschmidt A. Scale-free and multifractal time dynamics of fMRI signals during rest and task. Front. Physiol. 2012, 3:1-18. (Article 186).
17. Clauset A., Shalizi C., Newman M. Power law distributions in empirical data. SIAM Rev. 2009, 51:661-703.
18. Cole D., Smith S., Beckmann C. Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front. Syst. Neurosci. 2010, 4Apr:8.
19. Cordes D., Haughton V.M., Arfanakis K., Carew J.D., Turski P.A., Moritz C.H., Quigley M.A., Meyerand M.E. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. Am. J. Neuroradiol. 2001, 22(7):1326-1333.
20. 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(37):13848-13853.
21. Dehghani N., Hatsopoulos N.G., Haga Z.D., Parker R.A., Greger B., Halgren E., Cash S.S., Destexhe A. Avalanche analysis from multielectrode ensemble recordings in cat, monkey, and human cerebral cortex during wakefulness and sleep. Front. Physiol. 2012, 3 (Article 302).
22. Didier G., Pipiras V. Integral representations and properties of operator fractional Brownian motions. Bernoulli 2011, 17(1):1-33.
23. Dosenbach N.U., Visscher K.M., Palmer E.D., Miezin F.M., Wenger K.K., Kang H.C., Burgund E.D., Grimes A.L., Schlaggar B.L., Petersen S.E. A core system for the implementation of task sets. Neuron 2006, 50(5):799-812.
24. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E., Schlaggar B.L., Petersen S.E. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(26):11073-11078.
25. Embick D., Poeppel D. Mapping syntax using imaging: problems and prospects for the study of neurolinguistic computation. Encyclopedia of Language and Linguistics 2006, 484-486. Elsevier, Oxford, UK. 2nd edition. K. Brown (Ed.).
26. Expert P., Lambiotte R., Chialvo D.R., Christensen K., Jensen H.J., Sharp D.J., Turkheimer F. Self-similar correlation function in brain resting-state functional magnetic resonance imaging. J. R. Soc. Interface 2011, 8:472-479.
27. Fadili J., Bullmore E. Wavelet-generalized least squares: a new BLU estimator of linear regression models with 1/f errors. NeuroImage 2002, 15(1):217-232.
28. Feinberg D.A., Moeller S., Smith S.M., Auerbach E., Ramanna S., Glasser M.F., Miller K.L., Ugurbil K., Yacoub E. Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging. PLoS ONE 2010, 5:e15710.
29. Fox M., Raichle M. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
30. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(27):9673-9678.
31. Fox M.D., Corbetta M., Snyder A.Z., Vincent J.L., Raichle M.E. Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(26):10046-10051.
32. Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human evoked brain responses. Proc. Natl. Acad. Sci. U. S. A. 2007, 56(1):171-184.
33. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 1001:253-258.
34. He B.J. Scale-free properties of the functional magnetic resonance imaging signal during rest and task. J. Neurosci. 2011, 31(39):13786-13795.
35. He B.J. Spontaneous and task-evoked brain activity negatively interact. J. Neurosci. 2013, 33:4672-4682.
36. He B.J., Shulman G.L., Snyder A.Z., Corbetta M. The role of impaired neuronal communication in neurological disorders. Curr. Opin. Neurol. 2007, 20(6):655-660.
37. He B.J., Snyder A.Z., Vincent J.L., Epstein A., Shulman G.L., Corbetta M. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 2007, 53(6):905-918.
38. He B.J., Snyder A.Z., Zempel J.M., Smyth M.D., Raichle M.E. Electrophysiological correlates of the brain's instrinsic large-scale functional architecture. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(41):16039-16044.
39. He B.J., Zempel J.M., Snyder A.Z., Raichle M.E. The temporal structures and functional significance of scale-free brain activity. Neuron 2010, 66(3):353-369.
40. Helgason H., Pipiras V., Abry P. Fast and exact synthesis of stationary multivariate Gaussian time series using circulant embedding. Signal Process. 2011, 915:1123-1133.
41. Helgason H., Pipiras V., Abry P. Synthesis of multivariate stationary series with prescribed marginal distributions and covariance using circulant matrix embedding. Signal Process. 2011, 918:1741-1758.
42. Hlinka J., Palus M., Vejmelka M., Mantini D., Corbetta M. Functional connectivity in resting-state fMRI: is linear correlation sufficient?. NeuroImage 2011, 543:2218-2225.
43. Hutchison R.M., Womelsdorf T., Gati J.S., Everling S., Menon R.S. Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum. Brain Mapp. 2013, 34:2154-2177.
44. Kiviniemi V., Starck T., Remes J., Long X., Nikkinen J., Haapea M., Veijola J., Moilanen I., Isohanni M., Zang Y., et al. Functional segmentation of the brain cortex using high model order group PICA. Hum. Brain Mapp. 2009, 3012:3865-3886.
45. Kiviniemi V., Vire T., Remes J., Elseoud A.A., Starck T., Tervonen O., Nikkinen J. A sliding time-window ICA reveals spatial variability of the default mode network in time. Brain connect. 2011, 1:339-347.
46. Leonardi N., Richiardi J., Gschwind M., Simioni S., Annoni J.-M., Schluep M., Vuilleumier P., Van De Ville D. Principal components of functional connectivity: a new approach to study dynamic brain connectivity during rest. Neuroimage 2013 Dec, 83:937-950. Epub 2013 Jul 18. 10.1016/j.neuroimage.2013.07.019.
47. Lewis C.M., Baldassarre A., Committeri G., Romani G.L., Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(41):17558.
48. Linkenkaer-Hansen K., Nikouline V., Palva J., Ilmoniemi R. Long-range temporal correlations and scaling behavior in human brain oscillations. J. Neurosci. 2001, 21(4):1370-1377.
49. Liu X., Duyn J.H. Time-varying functional network information extracted from brief instances of spontaneous brain activity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4392-4397.
50. Majeed W., Magnuson M., Hasenkamp W., Schwarb H., Schumacher E.H., Barsalou L., Keilholz S. Spatiotemporal dynamics of low frequency BOLD fluctuations in rats and humans. NeuroImage 2011, 54:1140-1150.
51. Mallat S. A Wavelet Tour of Signal Processing 1998, Academic Press, San Diego, CA.
52. Marple S.L. Digital Spectral Analysis with Applications 1987, Prentice-Hall, Englewood Cliffs, NJ.
53. Marrelec G., Bellec P., Krainik A., Duffau H., Pélégrini-Issac M., Lehéricy S. Regions, systems, and the brain: hierarchical measures of functional integration in fMRI. Med. Image Anal. 2008, 124:484-496.
54. Maxim V., Sendur L., Fadili J., Suckling J., Gould R., Howard R., Bullmore E. Fractional Gaussian noise, functional MRI and Alzheimer's disease. NeuroImage 2005, 25(1):141-158.
55. Mendelbrot B.B., Van Ness J.W. Fractional Brownian motions, fractional noises and applications. SIAM Rev. 1968, 10:422-437.
56. Miller K.J., Sorensen L.B., Ojemann J.G., den Nijs M. Power-law scaling in the brain surface electric potential. PLoS Comput. Biol. 2009, 5:e1000609.
57. Mitchell J., Sundberg K., Reynolds J. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 2009, 63:879-888.
58. Moeller S., Yacoub E., Olman C.A., Auerbach E., Strupp J., Harel N., Ǔgurbil K. Multiband multislice GE-EPI at 7 Tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn. Reson. Med. 2010, 63(5):1144-1153.
59. Ojemann J.G., Akbudak E., Snyder A.Z., McKinstry R.C., Raichle M.E., Conturo T.E. Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. NeuroImage 1997, 6(3):156-167.
60. Rabrait C., Ciuciu P., Ribès A., Poupon C., Leroux P., Lebon V., Dehaene-Lambertz G., Le Bihan D., Lethimonnier F. High temporal resolution functional MRI using parallel echo volume imaging. J. Magn. Reson. Imaging 2008, 27(4):744-753.
61. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(2):676-682.
62. Sadaghiani G.Hesselmann, Friston K.J., Kleinschmidt A. The relation of ongoing brain activity, evoked neural responses, and cognition. Front. Syst. Neurosci. 2010, 4:20.
63. Salvador R., Suckling J., Schwarzbauer C., Bullmore E. Undirected graphs of frequency-dependent functional connectivity in whole brain networks. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2005, 3604:937-946.
64. Sasai S., Homae F., Watanabe H., Taga G. Frequency-specific functional connectivity in the brain during resting state revealed by NIRS. NeuroImage 2011, 56(1):252-257.
65. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27(9):2349-2356.
66. Shim W.H., Baek K., Kim J., Chae Y., Suh J., Rosen B.R., Jeong J., Kim Y.R. Frequency distribution of causal connectivity in rat sensorimotor network: resting-state fMRI analyses. J. Neurophysiol. 2013, 109(1):238-248.
67. Shimizu Y., Barth M., Windischberger C., Moser E., Thurner S. Wavelet-based multifractal analysis of fMRI time series. NeuroImage 2004, 22(3):1195-1202.
68. Shulman G.L., Fiez J.A., Corbetta M. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 1997, 9(5):648-663.
69. Siegel J., Power J., Dubis J., Vogel A., Church J., Schlaggar B., Petersen S. Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high-motion data points. Hum. Brain Mapp. 2013, 1-16.
70. Smith S., Fox P., Miller K., Glahn D., Fox P., Mackay C., Filippini N., Watkins K., Toro R., Laird A., et al. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040.
71. Smith S., Miller K., Moeller S., Xu J., Auerbach E.J., Woolrich M., Beckmann C., Jenkinson M., Andersson J., Glasser M., Van Essen D., Feinberg D., Yacoub E., Ugurbil K. Temporally-independent functional modes of spontaneous brain activity. Proc. Natl. Acad. Sci. U. S. A. 2012, 1098:3131-3136.
72. Stam C.J., de Bruin E.A. Scale-free dynamics of global functional connectivity in the human brain. Hum. Brain Mapp. 2004, 22(2):97-109.
73. Suckling J., Wink A.-M., Bernard F., Barnes A., Bullmore E. Endogenous multifractal brain dynamics are modulated by age, cholinergic blockade and cognitive performance. J. Neurosci. Methods 2008, 174(2):292-300.
74. Tagliazucchi E., Balenzuela P., Fraiman D., Chialvo D. Criticality in large-scale brain fMRI dynamics unveiled by a novel point process analysis. Front. Physiol. Artic. 2012, 15:1-12.
75. Tagliazucchi E., vonWegner F., Morzelewski A., Brodbeck V., Jahnke K., Laufs H. Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:15419-15424.
76. Talairach J., Tournoux P. Co-planar stereotaxic atlas of the human brain. 3-Dimensional Proportional System: An Approach to Cerebral Imaging 1988, Thieme Medical Publishers, Inc., Georg Thieme Verlag, Stuttgart, New York.
77. Thurner S., Windischberger E., Moser C., Walla P., Barth M. Scaling laws and persistence in human brain activity. Physica A 2003, 326(3):511-521.
78. Torres M.E., Abry P. Comparison of different methods for computing scaling parameter in the presence of trends. CD Memorias XIV Congreso Argentino de Bioingeniería y III Jornadas de Ingeniería Clínica (SABI 2003) 2003, Universitas, Córdoba, Argentina, (URL http://bioingenieria.edu.ar/grupos/ldnlys/metorres/metorres_files/SABI2003-074Torres.pdf).
79. Van de Ville D., Britz J., Michel C.M. EEG microstate sequences in healthy humans at rest reveal scale-free dynamics. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(42):18179-18184.
80. Veitch D., Abry P. A statistical test for the time constancy of scaling exponents. IEEE Trans. Sign. Process. 2001, 49(10):2325-2334.
81. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 2006, 96(6):3517-3531.
82. Vincent J.L., Kahn I., Snyder A.Z., Raichle M.E., Buckner R.L. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J. Neurophysiol. 2008, 100(6):3328-3342.
83. Wendt H., Abry P. Multifractality tests using bootstrapped wavelet leaders. IEEE Trans. Sign. Process. 2007, 55(10):4811-4820.
84. Wendt H., Scherrer A., Abry P., Achard S. Testing fractal connectivity in multivariate long memory processes. 34th Proc. IEEE ICASSP, Taipei, Taiwan 2009, 2913-2916.
85. Whitcher B., Guttorp P., Percival B.D. Wavelet analysis of covariance with application to atmospheric time series. J. Geophys. Res. Atmos. 2000, 105:14941-14962.
86. Wink A.-M., Bullmore E., Barnes A., Bernard F., Suckling J. Monofractal and multifractal dynamics of low frequency endogenous brain oscillations in functional MRI. Hum. Brain Mapp. 2008, 29(7):791-801.
87. Xiong J., Parsons L.M., Gao J.H., Fox P.T. Inter-regional connectivity to primary motor cortex revealed using MRI resting state images. Hum. Brain Mapp. 1999, 8(2-3):151-156.
88. Zarahn E., Aguirre G.K., D'Esposito M. Empirical analysis of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. NeuroImage 1997, 5(3):179-197.
89. Zhang D., Raichle M.E. Disease and the brain's dark energy, nature reviews. Neurology 2010, 6(1):15-28.
90. Zhang L., Qi R., Zhong J., Ni L., Zheng G., Xu J., Lu G. Disrupted functional connectivity of the anterior cingulate cortex in cirrhotic patients without overt hepatic encephalopathy: a resting state fMRI study. PLoS ONE 2013, 8(1):1-8. (Article e53206).
91. Zilber N., Ciuciu P., Abry P., van Wassenhove V. Modulation of scale-free properties of brain activity in MEG. Proc. of the 9th IEEE International Symposium on Biomedical Imaging, Barcelona, Spain 2012, 1531-1534.
92. Zilber N., Ciuciu P., Abry P., van Wassenhove V. Learning-induced modulation of scale-free properties of brain activity measured with MEG. 10th Proc. IEEE ISBI, San Francisco, CA 2013, 986-989.
93. Zilber N., Ciuciu P., Gramfort A., Azizi L., van Wassenhove V. Supramodal processing optimizes visual perceptual learning and plasticity. Neuroimage. 2014 Jun, 93(Pt 1):32-46.