Natural scenes viewing alters the dynamics of functional connectivity in the human brain

Neuron

Volumn 79, Issue 4, 2013, Pages 782-797

  Betti, Viviana ^a   DellaPenna, Stefania ^a   de Pasquale, Francesco ^a   Mantini, Dante ^b,c   Marzetti, Laura ^a   Romani, GianLuca ^a   Corbetta, Maurizio ^a,d  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ETH ZURICH   (Switzerland)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; BETA RHYTHM; BOLD SIGNAL; BRAIN FUNCTION; CORRELATION ANALYSIS; DEFAULT MODE NETWORK; DORSAL ATTENTION NETWORK; DYNAMICS; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMMA RHYTHM; HUMAN; LANGUAGE; MAGNETOENCEPHALOGRAPHY; MALE; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; OCCIPITAL CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; TASK PERFORMANCE; TOPOGRAPHY; VISION; VISUAL CORTEX;

ACOUSTIC STIMULATION; ADULT; ATTENTION; BRAIN; BRAIN MAPPING; ENVIRONMENT; EYE MOVEMENTS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; NERVE NET; NONLINEAR DYNAMICS; OXYGEN; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; PSYCHOPHYSICS; REST; SIGNAL PROCESSING, COMPUTER-ASSISTED; TIME FACTORS; VISUAL PATHWAYS; YOUNG ADULT;

EID: 84882638065     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.022     Document Type: Article

References (88)

1. Albert N.B., Robertson E.M., Miall R.C. The resting human brain and motor learning. Curr. Biol. 2009, 19:1023-1027.
2. Arfanakis K., Cordes D., Haughton V.M., Moritz C.H., Quigley M.A., Meyerand M.E. Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. Magn. Reson. Imaging 2000, 18:921-930.
3. Baldassarre A., Lewis C.M., Committeri G., Snyder A.Z., Romani G.L., Corbetta M. Individual variability in functional connectivity predicts performance of a perceptual task. Proc. Natl. Acad. Sci. USA 2012, 109:3516-3521.
4. Bartels A., Zeki S. Brain dynamics during natural viewing conditions-a new guide for mapping connectivity invivo. Neuroimage 2005, 24:339-349.
5. Berger H. On the electroencephalogram in man. Arch. Psychiatr. Nervenkr. 1929, 87:527-543.
6. Betti V., Zappasodi F., Rossini P.M., Aglioti S.M., Tecchio F. Synchronous with your feelings: sensorimotor gamma band and empathy for pain. J.Neurosci. 2009, 29:12384-12392.
7. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
8. Breshears J.D., Roland J.L., Sharma M., Gaona C.M., Freudenburg Z.V., Tempelhoff R., Avidan M.S., Leuthardt E.C. Stable and dynamic cortical electrophysiology of induction and emergence with propofol anesthesia. Proc. Natl. Acad. Sci. USA 2010, 107:21170-21175.
9. Brookes M.J., Hale J.R., Zumer J.M., Stevenson C.M., Francis S.T., Barnes G.R., Owen J.P., Morris P.G., Nagarajan S.S. Measuring functional connectivity using MEG: methodology and comparison with fcMRI. Neuroimage 2011, 56:1082-1104.
10. Brookes M.J., Woolrich M., Luckhoo H., Price D., Hale J.R., Stephenson M.C., Barnes G.R., Smith S.M., Morris P.G. Investigating the electrophysiological basis of resting state networks using magnetoencephalography. Proc. Natl. Acad. Sci. USA 2011, 108:16783-16788.
11. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J.Neurosci. 2009, 29:1860-1873.
12. Buzsáki G., Draguhn A. Neuronal oscillations in cortical networks. Science 2004, 304:1926-1929.
13. Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex. Science 2006, 313:1626-1628.
14. Capotosto P., Babiloni C., Romani G.L., Corbetta M. Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms. J.Neurosci. 2009, 29:5863-5872.
15. Chadick J.Z., Gazzaley A. Differential coupling of visual cortex with default or frontal-parietal network based on goals. Nat. Neurosci. 2011, 14:830-832.
16. de Pasquale F., Della Penna S., Snyder A.Z., Lewis C., Mantini D., Marzetti L., Belardinelli P., Ciancetta L., Pizzella V., Romani G.L., Corbetta M. Temporal dynamics of spontaneous MEG activity in brain networks. Proc. Natl. Acad. Sci. USA 2010, 107:6040-6045.
17. de Pasquale F., Della Penna S., Snyder A.Z., Marzetti L., Pizzella V., Romani G.L., Corbetta M. A cortical core for dynamic integration of functional networks in the resting human brain. Neuron 2012, 74:753-764.
18. Deco G., Corbetta M. The dynamical balance of the brain at rest. Neuroscientist 2011, 17:107-123.
19. Deco G., Jirsa V.K., McIntosh A.R. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat. Rev. Neurosci. 2011, 12:43-56.
20. Della Penna S., Del Gratta C., Granata C.G., Pasquarelli A., Pizzella V., Russo M., Torquati K., Erné S.N. Biomagnetic systems for clinical use. Philos. Mag. B 2000, 80:937-949.
21. Doucet G., Naveau M., Petit L., Delcroix N., Zago L., Crivello F., Jobard G., Tzourio-Mazoyer N., Mazoyer B., Mellet E., Joliot M. Brain activity at rest: a multiscale hierarchical functional organization. J.Neurophysiol. 2011, 105:2753-2763.
22. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
23. Fox M.D., Snyder A.Z., Zacks J.M., Raichle M.E. Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses. Nat. Neurosci. 2006, 9:23-25.
24. Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007, 56:171-184.
25. Fransson P. How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia 2006, 44:2836-2845.
26. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9:474-480.
27. Goense J.B., Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 2008, 18:631-640.
28. Goldman-Rakic P.S. Topography of cognition: parallel distributed networks in primate association cortex. Annu. Rev. Neurosci. 1988, 11:137-156.
29. Golland Y., Bentin S., Gelbard H., Benjamini Y., Heller R., Nir Y., Hasson U., Malach R. Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. Cereb. Cortex 2007, 17:766-777.
30. Greicius M.D., Menon V. Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. J.Cogn. Neurosci. 2004, 16:1484-1492.
31. 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. USA 2003, 100:253-258.
32. Greicius M.D., Kiviniemi V., Tervonen O., Vainionpää V., Alahuhta S., Reiss A.L., Menon V. Persistent default-mode network connectivity during light sedation. Hum. Brain Mapp. 2008, 29:839-847.
33. Greicius M.D., Supekar K., Menon V., Dougherty R.F. Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 2009, 19:72-78.
34. Gross J., Schnitzler A., Timmermann L., Ploner M. Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol. 2007, 5:e133.
35. Hacker C.D., Laumann T.O., Szrama N.P., Baldassarre A., Snyder A.Z., Leuthardt E.C., Corbetta M. Resting state network estimation in individual subjects. Neuroimage 2013, 82:616-633.
36. Hasson U., Nir Y., Levy I., Fuhrmann G., Malach R. Intersubject synchronization of cortical activity during natural vision. Science 2004, 303:1634-1640.
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, 53:905-918.
38. He B.J., Snyder A.Z., Zempel J.M., Smyth M.D., Raichle M.E. Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc. Natl. Acad. Sci. USA 2008, 105:16039-16044.
39. Hipp J.F., Engel A.K., Siegel M. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 2011, 69:387-396.
40. Hipp J.F., Hawellek D.J., Corbetta M., Siegel M., Engel A.K. Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat. Neurosci. 2012, 15:884-890.
41. Honey C.J., Kötter R., Breakspear M., Sporns O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl. Acad. Sci. USA 2007, 104:10240-10245.
42. Jensen O., Bonnefond M., VanRullen R. An oscillatory mechanism for prioritizing salient unattended stimuli. Trends Cogn. Sci. 2012, 16:200-206.
43. Kopell N., Ermentrout G.B., Whittington M.A., Traub R.D. Gamma rhythms and beta rhythms have different synchronization properties. Proc. Natl. Acad. Sci. USA 2000, 97:1867-1872.
44. Lakatos P., Karmos G., Mehta A.D., Ulbert I., Schroeder C.E. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 2008, 320:110-113.
45. Larson-Prior L.J., Zempel J.M., Nolan T.S., Prior F.W., Snyder A.Z., Raichle M.E. Cortical network functional connectivity in the descent to sleep. Proc. Natl. Acad. Sci. USA 2009, 106:4489-4494.
46. Lee M.H., Hacker C.D., Snyder A.Z., Corbetta M., Zhang D., Leuthardt E.C., Shimony J.S. Clustering of resting state networks. PLoS ONE 2012, 7:e40370.
47. Leopold D.A., Murayama Y., Logothetis N.K. Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb. Cortex 2003, 13:422-433.
48. 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. USA 2009, 106:17558-17563.
49. Liu Z., Fukunaga M., de Zwart J.A., Duyn J.H. Large-scale spontaneous fluctuations and correlations in brain electrical activity observed with magnetoencephalography. Neuroimage 2010, 51:102-111.
50. Mantini D., Della Penna S., Marzetti L., de Pasquale F., Pizzella V., Corbetta M., Romani G.L. A signal-processing pipeline for magnetoencephalography resting-state networks. Brain Connect 2011, 1:49-59.
51. Mantini D., Hasson U., Betti V., Perrucci M.G., Romani G.L., Corbetta M., Orban G.A., Vanduffel W. Interspecies activity correlations reveal functional correspondence between monkey and human brain areas. Nat. Methods 2012, 9:277-282.
52. Mantini D., Corbetta M., Romani G.L., Orban G.A., Vanduffel W. Evolutionarily novel functional networks in the human brain?. J.Neurosci. 2013, 33:3259-3275.
53. Marder E. Variability, compensation, and modulation in neurons and circuits. Proc. Natl. Acad. Sci. USA 2011, 108(Suppl 3):15542-15548.
54. Marzetti L., Della Penna S., Snyder A.Z., Pizzella V., Nolte G., de Pasquale F., Romani G.L., Corbetta M. Frequency specific interactions of MEG resting state activity within and across brain networks as revealed by the multivariate interaction measure. Neuroimage 2013, 79:172-183.
55. Mesulam M.M. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann. Neurol. 1990, 28:597-613.
56. Monto S., Palva S., Voipio J., Palva J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J.Neurosci. 2008, 28:8268-8272.
57. Morgan V.L., Price R.R. The effect of sensorimotor activation onfunctional connectivity mapping with MRI. Magn. Reson. Imaging 2004, 22:1069-1075.
58. Nauhaus I., Busse L., Carandini M., Ringach D.L. Stimulus contrast modulates functional connectivity in visual cortex. Nat. Neurosci. 2009, 12:70-76.
59. Nauhaus I., Busse L., Ringach D.L., Carandini M. Robustness oftraveling waves in ongoing activity of visual cortex. J.Neurosci. 2012, 32:3088-3094.
60. Nir Y., Hasson U., Levy I., Yeshurun Y., Malach R. Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation. Neuroimage 2006, 30:1313-1324.
61. Nir Y., Mukamel R., Dinstein I., Privman E., Harel M., Fisch L., Gelbard-Sagiv H., Kipervasser S., Andelman F., Neufeld M.Y., et al. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat. Neurosci. 2008, 11:1100-1108.
62. Nishimoto S., Vu A.T., Naselaris T., Benjamini Y., Yu B., Gallant J.L. Reconstructing visual experiences from brain activity evoked by natural movies. Curr. Biol. 2011, 21:1641-1646.
63. Raichle M.E. The restless brain. Brain Connect 2011, 1:3-12.
64. 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. USA 2001, 98:676-682.
65. Sauseng P., Gerloff C., Hummel F.C. Two brakes are better than one: the neural bases of inhibitory control of motor memory traces. Neuroimage 2013, 65:52-58.
66. Schoffelen J.M., Oostenveld R., Fries P. Neuronal coherence as a mechanism of effective corticospinal interaction. Science 2005, 308:111-113.
67. Schölvinck M.L., Maier A., Ye F.Q., Duyn J.H., Leopold D.A. Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. USA 2010, 107:10238-10243.
68. Schroeder C.E., Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 2009, 32:9-18.
69. Shulman G.L., Fiez J.A., Corbetta M., Buckner R.L., Miezin F.M., Raichle M.E., Petersen S.E. Common blood flow changes across visual tasks: 11. Decreases in cerebral cortex. J.Cogn. Neurosci. 1997, 9:648-663.
70. Siegel M., Donner T.H., Oostenveld R., Fries P., Engel A.K. Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 2008, 60:709-719.
71. Smith M.A., Kohn A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J.Neurosci. 2008, 28:12591-12603.
72. 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. USA 2009, 106:13040-13045.
73. 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. Temporally-independent functional modes of spontaneous brain activity. Proc. Natl. Acad. Sci. USA 2012, 109:3131-3136.
74. Sporns O. Networks of the Brain 2011, The MIT Press, Cambridge, MA.
75. Spreng R.N., Stevens W.D., Chamberlain J.P., Gilmore A.W., Schacter D.L. Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage 2010, 53:303-317.
76. Sridharan D., Levitin D.J., Chafe C.H., Berger J., Menon V. Neural dynamics of event segmentation in music: converging evidence for dissociable ventral and dorsal networks. Neuron 2007, 55:521-532.
77. Tambini A., Ketz N., Davachi L. Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 2010, 65:280-290.
78. Thut G., Nietzel A., Brandt S.A., Pascual-Leone A. Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J.Neurosci. 2006, 26:9494-9502.
79. Turrigiano G. Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 2011, 34:89-103.
80. VanRullen R., Koch C. Is perception discrete or continuous?. Trends Cogn. Sci. 2003, 7:207-213.
81. Varela F., Lachaux J.P., Rodriguez E., Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2001, 2:229-239.
82. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
83. von Stein A., Sarnthein J. Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 2000, 38:301-313.
84. Yeo B.T.T., Krienen F.M., Sepulcre J., Sabuncu M.R., Lashkari D., Hollinshead M., Roffman J.L., Smoller J.W., Zöllei L., Polimeni J.R., et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J.Neurophysiol. 2011, 106:1125-1165.
85. Zacks J.M., Swallow K.M. Event segmentation. Curr. Dir. Psychol. Sci. 2007, 16:80-84.
86. Zacks J.M., Braver T.S., Sheridan M.A., Donaldson D.I., Snyder A.Z., Ollinger J.M., Buckner R.L., Raichle M.E. Human brain activity time-locked to perceptual event boundaries. Nat. Neurosci. 2001, 4:651-655.
87. Zacks J.M., Speer N.K., Swallow K.M., Braver T.S., Reynolds J.R. Event perception: a mind-brain perspective. Psychol. Bull. 2007, 133:273-293.
88. Zanto T.P., Rubens M.T., Thangavel A., Gazzaley A. Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat. Neurosci. 2011, 14:656-661.