Different topological organization of human brain functional networks with eyes open versus eyes closed

NeuroImage

Volumn 90, Issue , 2014, Pages 246-255

  Xu, Pengfei ^a   Huang, Ruiwang ^a,b   Wang, Jinhui ^a   Van Dam, Nicholas T ^c   Xie, Teng ^a   Dong, Zhangye ^a   Chen, Chunping ^d   Gu, Ruolei ^d   Zang, Yu Feng ^a,e   He, Yong ^a   Fan, Jin ^f,g   Luo, Yue jia ^h  

^a BEIJING NORMAL UNIVERSITY   (China)

^b SOUTH CHINA NORMAL UNIVERSITY   (China)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUTE OF PSYCHOLOGY   (China)

^e HANGZHOU NORMAL UNIVERSITY   (China)

^f CITY UNIVERSITY OF NEW YORK   (United States)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^h SHENZHEN UNIVERSITY   (China)

Author keywords

Connectome; Exteroceptive; Graph theory; Interoceptive; Resting state functional MRI

Indexed keywords

CONNECTOME; EXTEROCEPTIVE; GRAPH THEORY; INTEROCEPTIVE; RESTING-STATE FUNCTIONAL MRI;

AWARENESS; BRAIN; BRAIN MAPPING; EYE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; REST; YOUNG ADULT;

EID: 84893524984     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.12.060     Document Type: Article

References (97)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3:174-183.
2. Astafiev S.V., Stanley C.M., Shulman G.L., Corbetta M. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat. Neurosci. 2004, 7:542-548.
3. Barry R.J., Clarke A.R., Johnstone S.J., Magee C.A., Rushby J.A. EEG differences between eyes-closed and eyes-open resting conditions. Clin. Neurophysiol. 2007, 118:2765-2773.
4. Bassett D.S., Bullmore E. Small-world brain networks. Neuroscientist 2006, 12:512-523.
5. Bechara A., Damasio H., Damasio A.R. Emotion, decision making and the orbitofrontal cortex. Cereb. Cortex 2000, 10:295-307.
6. Bianciardi M., Fukunaga M., van Gelderen P., Horovitz S.G., de Zwart J.A., Duyn J.H. Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. Neuroimage 2009, 45:160-168.
7. Binder J.R., Rao S.M., Hammeke T.A., Yetkin F.Z., Jesmanowicz A., Bandettini P.A., Wong E.C., Estkowski L.D., Goldstein M.D., Haughton V.M., Hyde J.S. Functional magnetic-resonance-imaging of human auditory-cortex. Ann. Neurol. 1994, 35:662-672.
8. Bogousslavsky J., Miklossy J., Deruaz J.P., Assal G., Regli F. Lingual and fusiform gyri in visual processing: a clinico-pathologic study of superior altitudinal hemianopia. J. Neurol. Neurosurg. Psychiatry 1987, 50:607-614.
9. Brandt T. How to see what you are looking for in fMRI and PET - or the crucial baseline condition. J. Neurol. 2006, 253:551-555.
10. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 2009, 10:186-198.
11. Burton H., Snyder A.Z., Raichle M.E. Default brain functionality in blind people. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15500-15505.
12. Celesia G.G. Organization of auditory cortical areas in man. Brain 1976, 99:403-414.
13. Chai X.J., Castanon A.N., Ongur D., Whitfield-Gabrieli S. Anticorrelations in resting state networks without global signal regression. Neuroimage 2012, 59:1420-1428.
14. Chai X.Q.J., Castanon A.N., Ongur D., Whitfield-Gabrieli S. Anticorrelations in resting state networks without global signal regression. Neuroimage 2012, 59:1420-1428.
15. Chen A.C., Feng W., Zhao H., Yin Y., Wang P. EEG default mode network in the human brain: spectral regional field powers. Neuroimage 2008, 41:561-574.
16. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
17. Craig A.D. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
18. Crick F., Koch C. A framework for consciousness. Nat. Neurosci. 2003, 6:119-126.
19. Critchley H.D. Electrodermal responses: what happens in the brain. Neuroscientist 2002, 8:132-142.
20. Critchley H.D. The human cortex responds to an interoceptive challenge. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6333-6334.
21. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7:189-195.
22. Critchley H.D., Nagai Y., Gray M.A., Mathias C.J. Dissecting axes of autonomic control in humans: insights from neuroimaging. Auton. Neurosci. 2011, 161:34-42.
23. Damasio A.R. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:1413-1420.
24. Downing P.E., Jiang Y., Shuman M., Kanwisher N. A cortical area selective for visual processing of the human body. Science 2001, 293:2470-2473.
25. Fan J., McCandliss B.D., Fossella J., Flombaum J.I., Posner M.I. The activation of attentional networks. Neuroimage 2005, 26:471-479.
26. Fan J., Xu P., Van Dam N.T., Eilam-Stock T., Gu X., Luo Y.J., Hof P.R. Spontaneous brain activity relates to autonomic arousal. J. Neurosci. 2012, 32:11176-11186.
27. Farb N.A., Segal Z.V., Anderson A.K. Attentional modulation of primary interoceptive and exteroceptive cortices. Cereb. Cortex 2013, 23:114-126.
28. Fox P.T., Burton H., Raichle M.E. Mapping human somatosensory cortex with positron emission tomography. J. Neurosurg. 1987, 67:34-43.
29. 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, 102:9673-9678.
30. 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, 103:10046-10051.
31. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 2009, 101:3270-3283.
32. Fransson P. Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum. Brain Mapp. 2005, 26:15-29.
33. Freeman L.C. A set of measures of centrality based on betweenness. Sociometry 1977, 40:35-41.
34. Friederici A.D., Ruschemeyer S.A., Hahne A., Fiebach C.J. The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. Cereb. Cortex 2003, 13:170-177.
35. Friston K. Beyond phrenology: what can neuroimaging tell us about distributed circuitry?. Annu. Rev. Neurosci. 2002, 25:221-250.
36. Griswold M.A., Jakob P.M., Heidemann R.M., Nittka M., Jellus V., Wang J., Kiefer B., Haase A. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn. Reson. Med. 2002, 47:1202-1210.
37. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., Sporns O. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6:e159.
38. He Y., Evans A. Graph theoretical modeling of brain connectivity. Curr. Opin. Neurol. 2010, 23:341-350.
39. He Y., Chen Z., Evans A. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J. Neurosci. 2008, 28:4756-4766.
40. Howard M.A., Volkov I.O., Mirsky R., Garell P.C., Noh M.D., Granner M., Damasio H., Steinschneider M., Reale R.A., Hind J.E., Brugge J.F. Auditory cortex on the human posterior superior temporal gyrus. J. Comp. Neurol. 2000, 416:79-92.
41. Hufner K., Stephan T., Glasauer S., Kalla R., Riedel E., Deutschlander A., Dera T., Wiesmann M., Strupp M., Brandt T. Differences in saccade-evoked brain activation patterns with eyes open or eyes closed in complete darkness. Exp. Brain Res. 2008, 186:419-430.
42. Hufner K., Stephan T., Flanagin V.L., Deutschlander A., Stein A., Kalla R., Dera T., Fesl G., Jahn K., Strupp M., Brandt T. Differential effects of eyes open or closed in darkness on brain activation patterns in blind subjects. Neurosci. Lett. 2009, 466:30-34.
43. Humphries M.D., Gurney K., Prescott T.J. The brainstem reticular formation is a small-world, not scale-free, network. Proc. Biol. Sci. 2006, 273:503-511.
44. Jao T., Vertes P.E., Alexander-Bloch A.F., Tang I.N., Yu Y.C., Chen J.H., Bullmore E.T. Volitional eyes opening perturbs brain dynamics and functional connectivity regardless of light input. Neuroimage 2013, 69:21-34.
45. Latora V., Marchiori M. Efficient behavior of small-world networks. Phys. Rev. Lett. 2001, 87:198701.
46. Machielsen W.C., Rombouts S.A., Barkhof F., Scheltens P., Witter M.P. FMRI of visual encoding: reproducibility of activation. Hum. Brain Mapp. 2000, 9:156-164.
47. Marx E., Stephan T., Nolte A., Deutschländer A., Seelos K.C., Dieterich M., Brandt T. Eye closure in darkness animates sensory systems. Neuroimage 2003, 19:924-934.
48. Marx E., Deutschlander A., Stephan T., Dieterich M., Wiesmann M., Brandt T. Eyes open and eyes closed as rest conditions: impact on brain activation patterns. Neuroimage 2004, 21:1818-1824.
49. Maslov S., Sneppen K. Specificity and stability in topology of protein networks. Science 2002, 296:910-913.
50. McAvoy M., Larson-Prior L., Nolan T.S., Vaishnavi S.N., Raichle M.E., d'Avossa G. Resting states affect spontaneous BOLD oscillations in sensory and paralimbic cortex. J. Neurophysiol. 2008, 100:922-931.
51. McAvoy M., Larson-Prior L., Ludwikow M., Zhang D., Snyder A.Z., Gusnard D.L., Raichle M.E., d'Avossa G. Dissociated mean and functional connectivity BOLD signals in visual cortex during eyes closed and fixation. J. Neurophysiol. 2012, 108:2363-2372.
52. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., Alon U. Network motifs: simple building blocks of complex networks. Science 2002, 298:824-827.
53. Mowinckel A.M., Espeseth T., Westlye L.T. Network-specific effects of age and in-scanner subject motion: a resting-state fMRI study of 238 healthy adults. Neuroimage 2012, 63:1364-1373.
54. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage 2009, 44:893-905.
55. Nakano T., Kato M., Morito Y., Itoi S., Kitazawa S. Blink-related momentary activation of the default mode network while viewing videos. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:702-706.
56. Newman M.E.J. The structure and function of complex networks. SIAM Rev. 2003, 45:167-256.
57. 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.
58. Niven J.E., Laughlin S.B. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 2008, 211:1792-1804.
59. Nobre A.C., Sebestyen G.N., Gitelman D.R., Mesulam M.M., Frackowiak R.S.J., Frith C.D. Functional localization of the system for visuospatial attention using positron emission tomography. Brain 1997, 120:515-533.
60. Power J.D., Cohen A.L., Nelson S.M., Wig G.S., Barnes K.A., Church J.A., Vogel A.C., Laumann T.O., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional network organization of the human brain. Neuron 2011, 72:665-678.
61. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
62. 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, 98:676-682.
63. Rizzolatti G., Luppino G. The cortical motor system. Neuron 2001, 31:889-901.
64. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010, 52:1059-1069.
65. Saad Z.S., Gotts S.J., Murphy K., Chen G., Jo H.J., Martin A., Cox R.W. Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2012, 2:25-32.
66. Satterthwaite T.D., Wolf D.H., Loughead J., Ruparel K., Elliott M.A., Hakonarson H., Gur R.C., Gur R.E. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 2012, 60:623-632.
67. Scholvinck 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. U. S. A. 2010, 107:10238-10243.
68. Sepulcre J., Liu H., Talukdar T., Martincorena I., Yeo B.T., Buckner R.L. The organization of local and distant functional connectivity in the human brain. PLoS Comput. Biol. 2010, 6:e1000808.
69. Simmons W.K., Avery J.A., Barcalow J.C., Bodurka J., Drevets W.C., Bellgowan P. Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness. Hum. Brain Mapp. 2014, 34:2944-2958.
70. Sporns O., Kötter R. Motifs in brain networks. PLoS Biol. 2004, 2:e369.
71. Sporns O., Zwi J.D. The small world of the cerebral cortex. Neuroinformatics 2004, 2:145-162.
72. Sporns O., Chialvo D.R., Kaiser M., Hilgetag C.C. Organization, development and function of complex brain networks. Trends Cogn. Sci. 2004, 8:418-425.
73. Tian L., Wang J., Yan C., He Y. Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. Neuroimage 2011, 54:191-202.
74. Tononi G., Edelman G.M., Sporns O. Complexity and coherency: integrating information in the brain. Trends Cogn. Sci. 1998, 2:474-484.
75. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
76. Urgesi C., Candidi M., Ionta S., Aglioti S.M. Representation of body identity and body actions in extrastriate body area and ventral premotor cortex. Nat. Neurosci. 2007, 10:30-31.
77. Van Dijk K.R., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010, 103:297-321.
78. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
79. Van Essen D.C. Visual areas of the mammalian cerebral cortex. Annu. Rev. Neurosci. 1979, 2:227-263.
80. Wang J., Wang L., Zang Y., Yang H., Tang H., Gong Q., Chen Z., Zhu C., He Y. Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum. Brain Mapp. 2009, 30:1511-1523.
81. Wang J., Zuo X., He Y. Graph-based network analysis of resting-state functional MRI. Front. Syst. Neurosci. 2010, 4:16.
82. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
83. Watts D.J., Strogatz S.H. Collective dynamics of'small-world'networks. Nature 1998, 393:440-442.
84. Weissenbacher A., Kasess C., Gerstl F., Lanzenberger R., Moser E., Windischberger C. Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. Neuroimage 2009, 47:1408-1416.
85. Wiesmann M., Kopietz R., Albrecht J., Linn J., Reime U., Kara E., Pollatos O., Sakar V., Anzinger A., Fesl G., Bruckmann H., Kobal G., Stephan T. Eye closure in darkness animates olfactory and gustatory cortical areas. Neuroimage 2006, 32:293-300.
86. Wig G.S., Schlaggar B.L., Petersen S.E. Concepts and principles in the analysis of brain networks. Ann. N. Y. Acad. Sci. 2011, 1224:126-146.
87. Xia M., Wang J., He Y. BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 2013, 8:e68910.
88. Yan C.-G., Zang Y.-F. DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Front. Syst. Neurosci. 2010, 4:13.
89. Yan C., Liu D., He Y., Zou Q., Zhu C., Zuo X., Long X., Zang Y. Spontaneous brain activity in the default mode network is sensitive to different resting-state conditions with limited cognitive load. PLoS One 2009, 4:e5743.
90. Yan C.G., Craddock R.C., Zuo X.N., Zang Y.F., Milham M.P. Standardizing the intrinsic brain: towards robust measurement of inter-individual variation in 1000 functional connectomes. Neuroimage 2013, 80:246-262.
91. Yang H., Long X.Y., Yang Y., Yan H., Zhu C.Z., Zhou X.P., Zang Y.F., Gong Q.Y. Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage 2007, 36:144-152.
92. Zalesky A., Fornito A., Bullmore E.T. Network-based statistic: identifying differences in brain networks. Neuroimage 2010, 53:1197-1207.
93. Zalesky A., Fornito A., Harding I.H., Cocchi L., Yucel M., Pantelis C., Bullmore E.T. Whole-brain anatomical networks: does the choice of nodes matter?. Neuroimage 2010, 50:970-983.
94. Zalesky A., Fornito A., Bullmore E. On the use of correlation as a measure of network connectivity. Neuroimage 2012, 60:2096-2106.
95. Zeki S., Shipp S. The functional logic of cortical connections. Nature 1988, 335:311-317.
96. Zou Q., Long X., Zuo X., Yan C., Zhu C., Yang Y., Liu D., He Y., Zang Y. Functional connectivity between the thalamus and visual cortex under eyes closed and eyes open conditions: a resting-state fMRI study. Hum. Brain Mapp. 2009, 30:3066-3078.
97. Zuo X.N., Xu T., Jiang L., Yang Z., Cao X.Y., He Y., Zang Y.F., Castellanos F.X., Milham M.P. Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. Neuroimage 2013, 65:374-386.