On the Stability of BOLD fMRI Correlations

Cerebral Cortex

Volumn 27, Issue 10, 2017, Pages 4719-4732

  Laumann, Timothy O ^a   Snyder, Abraham Z ^a   Mitra, Anish ^a   Gordon, Evan M ^b,c   Gratton, Caterina ^a   Adeyemo, Babatunde ^a   Gilmore, Adrian W ^d   Nelson, Steven M ^b,c   Berg, Jeff J ^d   Greene, Deanna J ^a   McCarthy, John E ^d   Tagliazucchi, Enzo ^a   Laufs, Helmut ^a,e   Schlaggar, Bradley L ^a,e,f   Dosenbach, Nico U F ^a   Petersen, Steven E ^a,d,e  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VISN 17 Center of Excellence for Research on Returning War Veterans   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e UNIVERSITY OF KIEL   (Germany)

^f GOETHE UNIVERSITY   (Germany)

Author keywords

BOLD fMRI; dynamics; functional connectivity; nonstationarity; resting state

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; CORRELATIONAL STUDY; DROWSINESS; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEAD MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RESTING STATE NETWORK; SAMPLING ERROR; SLEEP STAGE; TIME SERIES ANALYSIS; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; IMAGE PROCESSING; METABOLISM; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; REST; YOUNG ADULT;

OXYGEN;

ADULT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; REST; YOUNG ADULT;

EID: 85030163732     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw265     Document Type: Article

References (94)

1. Al-Aidroos N, Said CP, Turk-Browne NB. 2012. Top-down attention switches coupling between low-level and high-level areas of human visual cortex. Proc Natl Acad Sci USA. 109 (36): 14675-14680.
2. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD. 2014. Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex. 24 (3): 663-676.
3. Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S. 2015. Signature of consciousness in the dynamics of resting-state brain activity. Proc Natl Acad Sci USA. 112 (3): 887-892.
4. Bianciardi M, Fukunaga M, van Gelderen P, Horovitz SG, de Zwart JA, Duyn JH. 2009. Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. Neuroimage. 45 (1): 160-168.
5. Bishop GH. 1932. Cyclic changes in excitability of the optic pathway of the rabbit. Am J Physiol. 103: 213-224.
6. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. 1995. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 34 (4): 537-541.
7. Calhoun VD, Miller R, Pearlson G, Adali T. 2014. The chronnectome: time-varying connectivity networks as the next frontier in fMRI data discovery. Neuron. 84 (2): 262-274.
8. Chang C, Glover GH. 2010. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage. 50 (1): 81-98.
9. Chang C, Leopold DA, Scholvinck ML, Mandelkow H, Picchioni D, Liu X, Ye FQ, Turchi JN, Duyn JH. 2016. Tracking brain arousal fluctuations with fMRI. Proc Natl Acad Sci USA. 113 (16): 4518-4523.
10. Chen B, Xu T, Zhou C, Wang L, Yang N, Wang Z, Dong HM, Yang Z, Zang YF, Zuo XN, et al. 2015. Individual variability and test-retest reliability revealed by ten repeatedresting-state brain scans over one month. PLoS One. 10 (12): e0144963.
11. Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE. 2014. Intrinsic and task-evoked network architectures of the human brain. Neuron. 83 (1): 238-251.
12. Cordes D, Nandy RR. 2006. Estimation of the intrinsic dimensionality of fMRI data. Neuroimage. 103 (29): 145-154.
13. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF. 2006. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA. 103 (37): 13848-13853.
14. Deco G, Rolls ET, Romo R. 2009. Stochastic dynamics as a principle of brain function. Prog Neurobiol. 88 (1): 1-16.
15. Dement W, Kleitman N. 1957. The relation of eye movements during sleep to dream activity: An objective method for the study of dreaming. J Exp Psychol. 53 (5): 339-346.
16. Dubis JW, Siegel JS, Neta M, Visscher KM, Petersen SE. 2016. Tasks driven by perceptual information do not recruit sustained BOLD activity in Cingulo-Opercular Regions. Cereb Cortex. 26 (1): 192-201.
17. Fox MD, Snyder AZ, Vincent JL, Raichle ME. 2007. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron. 56 (1): 171-184.
18. Fransson P. 2006. How default is the default mode of brain function Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia. 44 (14): 2836-2845.
19. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. 1997. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 6 (3): 218-229.
20. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R. 1996. Movement-related effects in fMRI time-series. Magn Reson Med. 35 (3): 346-355.
21. Gonzalez-Castillo J, Hoy CW, Handwerker DA, Robinson ME, Buchanan LC, Saad ZS, Bandettini PA. 2015. Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns. Proc Natl Acad Sci USA. 112 (28): 8762-8767.
22. Gordon EM, Laumann TO, Adeyemo B, Huckins JF, Kelley WM, Petersen SE. 2016. Generation and evaluation of a cortical area parcellation from resting-state correlations. Cereb Cortex. 26 (1): 288-303.
23. Halliday DM, Rosenberg JR, Rigas A, Conway BA. 2009. A periodogram-based test for weak stationarity and consistency between sections in time series. J Neurosci Methods. 180 (1): 138-146.
24. Haxby JV, Connolly AC, Guntupalli JS. 2014. Decoding neural representational spaces using multivariate pattern analysis. Annu Rev Neurosci. 37: 435-456.
25. He BJ. 2013. Spontaneous and task-evoked brain activity negatively interact. J Neurosci. 33 (11): 4672-4682.
26. He BJ, Zempel JM, Snyder AZ, Raichle ME. 2010. The temporal structures and functional significance of scale-free brain activity. Neuron. 66 (3): 353-369.
27. Henze N. 2002. Invariant test for multivariate normality: A critical review. Stat Papers. 43: 467-506.
28. Hesselmann G, Kell CA, Kleinschmidt A. 2008. Ongoing activity fluctuations in hMT+ bias the perception of coherent visual motion. J Neurosci. 28 (53): 14481-14485.
29. Hindriks R, Adhikari MH, Murayama Y, Ganzetti M, Mantini D, Logothetis NK, Deco G. 2016. Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI Neuroimage. 127: 242-256
30. Hlinka J, Hadrava M. 2015. On the danger of detecting network states in white noise. Front Comput Neurosci. 9: 11.
31. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P. 2009. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA. 106 (6): 2035-2040.
32. Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH. 2009. Decoupling of the brain's default mode network during deep sleep. Proc Natl Acad Sci USA. 106 (27): 11376-11381.
33. Hutchison RM, Morton JB. 2015. Tracking the brain's functional coupling dynamics over development. J Neurosci. 35 (17): 6849-6859.
34. Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta M, Della Penna S, Duyn JH, Glover GH, Gonzalez-Castillo J, et al. 2013a. Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage. 80: 360-378.
35. Hutchison RM, Womelsdorf T, Gati JS, Everling S, Menon RS. 2013b. Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum Brain Mapp. 34: 2154-2177.
36. Jentsch C, Subba Rao S. 2015. A test for second order stationarity of a multivariate time series. J Economet. 185: 124-161.
37. Karahanoglu FI, Van De Ville D. 2015. Transient brain activity disentangles fMRI resting-state dynamics in terms of spatially and temporally overlapping networks. Nat Commun. 6: 7751.
38. Kirkby LA, Sack GS, Firl A, Feller MB. 2013. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron. 80 (5): 1129-1144.
39. Kopell NJ, Gritton HJ, Whittington MA, Kramer MA. 2014. Beyond the connectome: the dynome. Neuron. 83 (6): 1319-1328.
40. Krienen FM, Yeo BT, Buckner RL. 2014. Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture. Philos Trans R Soc Lond B Biol Sci. 369 (1653).
41. Kullmann DM, Moreau AW, Bakiri Y, Nicholson E. 2012. Plasticity of inhibition. Neuron. 75 (6): 951-962.
42. Last M, Shumway R. 2008. Detecting abrupt changes in a piecewise locally stationary time series. J Multivar Anal. 99 (2): 191-214.
43. Laumann TO, Gordon EM, Adeyemo B, Snyder AZ, Joo SJ, Chen MY, Gilmore AW, McDermott KB, Nelson SM, Dosenbach NU, et al. 2015. Functional system and areal organization of a highly sampled individual human brain. Neuron. 87 (3): 657-670.
44. Leonardi N, Van De Ville D. 2015. On spurious and real fluctuations of dynamic functional connectivity during rest. Neuroimage. 104: 430-436.
45. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M. 2009. Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci USA. 106 (41): 17558-17563.
46. Lindquist MA, Xu Y, Nebel MB, Caffo BS. 2014. Evaluating dynamic bivariate correlations in resting-state fMRI: A comparison study and a new approach. Neuroimage. 101: 531-546.
47. Liu X, Duyn JH. 2013. Time-varying functional network information extracted from brief instances of spontaneous brain activity. Proc Natl Acad Sci USA. 110 (11): 4392-4397.
48. Lu J, Liu H, Zhang M, Wang D, Cao Y, Ma Q, Rong D, Wang X, Buckner RL, Li K. 2011. Focal pontine lesions provide evidence that intrinsic functional connectivity reflects polysynaptic anatomical pathways. J Neurosci. 31 (42): 15065-15071.
49. Malenka RC, Bear MF. 2004. LTP and LTD: An embarrassment of riches. Neuron. 44 (1): 5-21.
50. Marder E, Goaillard JM. 2006. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 7 (7): 563-574.
51. Mardia KV. 1970. Measures of multivariate skewness and kurtosis with applications. Biometrika. 57 (3): 519-530.
52. Martins ACR. 2007. Non-stationary correlation matrices and noise. Phys A. 379: 552-558.
53. McAvoy M, Larson-Prior L, Nolan TS, Vaishnavi SN, Raichle ME, d'Avossa G. 2008. Resting states affect spontaneous BOLD oscillations in sensory and paralimbic cortex. J Neurophysiol. 100 (2): 922-931.
54. Mhuircheartaigh RN, Rosenorn-Lanng D, Wise R, Jbabdi S, Rogers R, Tracey I. 2010. Cortical and subcortical connectivity changes during decreasing levels of consciousness in humans: A functional magnetic resonance imaging study using propofol. J Neurosci. 30 (27): 9095-9102.
55. Mitra A, Snyder AZ, Blazey T, Raichle ME. 2015a. Lag threads organize the brain's intrinsic activity. Proc Natl Acad Sci USA. 112 (17): E2235-2244.
56. Mitra A, Snyder AZ, Constantino JN, Raichle ME. 2017. The lag structure of intrinsic activity is focally altered in high functioning adults with autism. Cereb Cortex. 27: 1083-1093
57. Mitra A, Snyder AZ, Hacker CD, Raichle ME. 2014. Lag structure in resting-state fMRI. J Neurophysiol. 111 (11): 2374-2391.
58. Mitra A, Snyder AZ, Tagliazucchi E, Laufs H, Raichle ME. 2015b. Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep. Elife. 4: e10781.
59. Nahmani M, Turrigiano GG. 2014. Adult cortical plasticity following injury: recapitulation of critical period mechanisms Neuroscience. 283: 4-16.
60. O'Reilly JX, Croxson PL, Jbabdi S, Sallet J, Noonan MP, Mars RB, Browning PG, Wilson CR, Mitchell AS, Miller KL, et al. 2013. Causal effect of disconnection lesions on interhemispheric functional connectivity in rhesus monkeys. Proc Natl Acad Sci USA. 110 (34): 13982-13987.
61. Palanca BJ, Mitra A, Larson-Prior L, Snyder AZ, Avidan MS, Raichle ME. 2015. Resting-state functional magnetic resonance imaging correlates of sevoflurane-induced unconsciousness. Anesthesiology. 123 (2): 346-356.
62. Penn AA, Shatz CJ. 1999. Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatr Res. 45 (4 Pt 1): 447-458.
63. Picchioni D, Duyn JH, Horovitz SG. 2013. Sleep and the functional connectome. Neuroimage. 80: 387-396.
64. Poldrack RA, Laumann TO, Koyejo O, Gregory B, Hover A, Chen MY, Luci J, Huk A, Joo SJ, Boyd R, et al. 2015. Long-term neural and physiological phenotyping of a single human. Nat Comm. 6: 8885
65. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. 2012. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 59 (3): 2142-2154.
66. Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL, et al. 2011. Functional network organization of the human brain. Neuron. 72 (4): 665-678.
67. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. 2014. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage. 84: 320-341.
68. Raichle ME, Snyder AZ. 2007. A default mode of brain function: A brief history of an evolving idea. Neuroimage. 37 (4): 1083-1090discussion 1097-1089.
69. Rosvall M, Bergstrom CT. 2008. Maps of random walks on complex networks reveal community structure. Proc Natl Acad Sci USA. 105 (4): 1118-1123.
70. Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud AL, Kleinschmidt A. 2010. Intrinsic connectivity networks, alpha oscillations, and tonic alertness: A simultaneous electroencephalography/ functional magnetic resonance imaging study. J Neurosci. 30 (30): 10243-10250.
71. Salek-Haddadi A, Diehl B, Hamandi K, Merschhemke M, Liston A, Friston K, Duncan JS, Fish DR, Lemieux L. 2006. Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy. Brain Res. 1088 (1): 148-166.
72. Samann PG, Wehrle R, Hoehn D, Spoormaker VI, Peters H, Tully C, Holsboer F, Czisch M. 2011. Development of the brain's default mode network from wakefulness to slow wave sleep. Cereb Cortex. 21 (9): 2082-2093.
73. Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE. 2012. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage. 60 (1): 623-632.
74. Schacher S, Hu JY. 2014. The less things change, the more they are different: contributions of long-term synaptic plasticity and homeostasis to memory. Learn Mem. 21 (3): 128-134.
75. Shehzad Z, Kelly AM, Reiss PT, Gee DG, Gotimer K, Uddin LQ, Lee SH, Margulies DS, Roy AK, Biswal BB, et al. 2009. The resting brain: unconstrained yet reliable. Cereb Cortex. 19 (10): 2209-2229.
76. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, et al. 2009. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA. 106 (31): 13040-13045.
77. Tagliazucchi E, Balenzuela P, Fraiman D, Chialvo DR. 2012a. Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. Front Physiol. 3: 15.
78. Tagliazucchi E, Laufs H. 2014. Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron. 82 (3): 695-708.
79. Tagliazucchi E, vonWegner F, Morzelewski A, Borisov S, Jahnke K, Laufs H. 2012b. Automatic sleep staging using fMRI functional connectivity data. Neuroimage. 63 (1): 63-72.
80. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Jahnke K, Laufs H. 2013. Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc Natl Acad Sci USA. 110 (38): 15419-15424.
81. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Laufs H. 2012c. Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front Hum Neurosci. 6: 339.
82. Takesian AE, Hensch TK. 2013. Balancing plasticity/stability across brain development. Prog Brain Res. 207: 3-34.
83. Turrigiano G. 2012. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol. 4 (1): A005736.
84. Van Dijk KR, Sabuncu MR, Buckner RL. 2012. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage. 59 (1): 431-438.
85. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME. 2007. Intrinsic functional architecture in the anaesthetized monkey brain. Nature. 447 (7140): 83-86.
86. Vitureira N, Goda Y. 2013. Cell biology in neuroscience: the interplay between Hebbian and homeostatic synaptic plasticity. J Cell Biol. 203 (2): 175-186.
87. Weatherburn CE. 1961. A first course in mathematical statistics. 3rd ed. London: Cambridge University Press.
88. Wong KF, Galka A, Yamashita O, Ozaki T. 2006. Modelling non-stationary variance in EEG time series by state space GARCH model. Comput Biol Med. 36 (12): 1327-1335.
89. Yan CG, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A, Li Q, Zuo XN, Castellanos FX, Milham MP. 2013. A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage. 76: 183-201.
90. Yang Z, Huang Z, Gonzalez-Castillo J, Dai R, Northoff G, Bandettini P. 2014. Using fMRI to decode true thoughts independent of intention to conceal. Neuroimage. 99: 80-92.
91. Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zollei L, Polimeni JR, et al. 2011. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 106 (3): 1125-1165.
92. Zalesky A, Breakspear M. 2015. Towards a statistical test for functional connectivity dynamics. Neuroimage. 114: 466-470.
93. Zalesky A, Fornito A, Cocchi L, Gollo LL, Breakspear M. 2014. Time-resolved resting-state brain networks. Proc Natl Acad Sci USA. 111 (28): 10341-10346.
94. Zuo XN, Xing XX. 2014. Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective. Neurosci Biobehav Rev. 45: 100-118.