Simultaneous EEG-fMRI reveals a temporal cascade of task-related and default-mode activations during a simple target detection task

NeuroImage

Volumn 102, Issue P1, 2014, Pages 229-239

  Walz, Jennifer M ^a   Goldman, Robin I ^a,b   Carapezza, Michael ^a   Muraskin, Jordan ^a   Brown, Truman R ^c   Sajda, Paul ^a  

^a Columbia University Department of Biomedical Engineering ^*  (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Attention modulation; Default mode network; EEG; FMRI; Multi modal imaging; Single trial variability

Indexed keywords

ADULT; ARTICLE; ATTENTION; BOLD SIGNAL; BRAIN MAPPING; DEFAULT MODE NETWORK; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; MULTIMODAL IMAGING; NEUROMODULATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; ORIENTATION; POSTERIOR CINGULATE; PRECUNEUS; RECEIVER OPERATING CHARACTERISTIC; TASK PERFORMANCE; VALIDATION PROCESS; YOUNG ADULT; BRAIN; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; TIME;

ADULT; ATTENTION; BRAIN; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MULTIMODAL IMAGING; NEUROIMAGING; TASK PERFORMANCE AND ANALYSIS; TIME FACTORS; YOUNG ADULT;

EID: 84908368791     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.08.014     Document Type: Article

References (73)

1. Benar C.-G., Schon D., Grimault S., Nazarian B., Burle B., Roth M., Badier J.-M., Marquis P., Liegeois-Chauvel C., Anton J.-L. Single-trial analysis of oddball event-related potentials in simultaneous EEG-fMRI. Hum. Brain Mapp. 2007, 28:602-613.
2. Bianciardi M., Fukunaga M., van Gelderen P., de Zwart J.A., Duyn J.H. Negative BOLD-fMRI signals in large cerebral veins. J. Cereb. Blood Flow Metab. 2011, 31:401-412.
3. Bledowski C., Prvulovic D., Goebel R., Zanella F.E., Linden D.E. Attentional systems in target and distractor processing: a combined ERP and fMRI study. NeuroImage 2004, 22:530-540.
4. Bledowski C., Prvulovic D., Hoechstetter K., Scherg M., Wibral M., Goebel R., Linden D.E.J. Localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. J. Neurosci. 2004, 24(42):9353-9360.
5. Boly M., Balteau E., Schnakers C., Degueldre C., Moonen G., Luxen A., Phillips C., Peigneux P., Maquet P., Laureys S. Baseline brain activity fluctuations predict somatosensory perception in humans. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(29):12187-12192.
6. Bressler S.L., Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn. Sci. 2010, 14:277-290.
7. 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. U. S. A. 2011, 108(40):16783-16788.
8. Cavanna A.E., Trimble M.R. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 2006, 129:564-583.
9. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:215-229.
10. Corbetta M., Patel G.H., Shulman G.L. The reorienting system of the human brain: from environment to theory of mind. Neuron 2008, 58:306-324.
11. Crottaz-Herbette S., Menon V. Where and when the anterior cingulate cortex modulates attentional response: combined fMRI and ERP evidence. J. Cogn. Neurosci. 2006, 18(5):766-780.
12. De Luca M., Beckmann C.F., De Stefano N., Matthews P.M., Smith S.M. fMRI resting state networks define distinct modes of long-distance interactions in the human brain. NeuroImage 2006, 29(4):1359-1367.
13. de Pasquale F., Penna S.D., 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. U. S. A. 2010, 107(13):6040-6045.
14. deBettencourt M., Goldman R.I., Brown T.R., Sajda P. Adaptive thresholding for improving sensitivity in single-trial simultaneous EEG/fMRI. Front. Psychol. 2011, 2:91.
15. Duda R.O., Hart P.E., Stork D.G. Pattern Classification 2001, Wiley, New York.
16. Eason R.G., Harter M.R., White T.C. Effects of attention and arousal on visually evoked cortical potentials and reaction time in man. Physiol. Behav. 1969, 4(3):283-289.
17. Eichele T., Specht K., Moosmann M., Jongsma M.L.A., Quiroga R.Q., Nordby H., Hugdahl K. Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(49):17798-17803.
18. Eichele T., Debener S., Calhoun V.D., Specht K., Engel A.K., Hugdahl K., von Cramen D.Y., Ullsperger M. Prediction of human errors by maladaptive changes in event-related brain networks. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(16):6173-6178.
19. Esposito F., Bertolino A., Scarabino T., Latorre V., Blasi G., Popolizio T., Tedeschi G., Cirillo S., Goebel R., Di Salle F. Independent component model of the default-mode brain function: assessing the impact of active thinking. Brain Res. Bull. 2006, 70(4-6):263-269.
20. Esposito F., Aragri A., Piccoli T., Tedeschi G., Goebel R., Di Salle F. Distributed analysis of simultaneous EEG-fMRI time-series: modeling and interpretation issues. Magn. Reson. Imaging 2009, 27:1120-1130.
21. Esposito F., Mulert C., Goebel R. Combined distributed source and single-trial EEG-fMRI modeling: application to effortful decision making processes. NeuroImage 2009, 47:112-121.
22. Feige B., Scheffler K., Esposito F., Di Salle F., Hennig J., Seifritz E. Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. J. Neurophysiol. 2005, 93:2864-2872.
23. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8(9):700-711.
24. Fuster J.M. The prefrontal cortex-an update: time is of the essence. Neuron 2001, 30:319-333.
25. Gerson A.D., Parra L.C., Sajda P. Cortical origins of response time variability during rapid discrimination of visual objects. NeuroImage 2005, 28:342-353.
26. Ghez C., Fahn S. The cerebellum. Principles of Neural Science 1985, 502-522. Elsevier, New York. 2nd ed. E.R. Kandel, J.H. Schwartz (Eds.).
27. Goldberg I., Harel M., Malach R. When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 2006, 50(2):329-339.
28. Goldman R.I., Stern J.M., Engel J., Cohen M.S. Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport 2002, 13(18):2487-2492.
29. Goldman R.I., Wei C.-Y., Philiastides M.G., Gerson A.D., Friedman D., Brown T.R., Sajda P. Single-trial discrimination for integrating simultaneous EEG and fMRI: Identifying cortical areas for trial-to-trial variability in the auditory oddball task. NeuroImage 2009, 27:136-147.
30. Green D.M., Swets J.A. Signal Detection Theory and Psychophysics 1966, Wiley, New York.
31. Hopfinger J.B., West V.M. Interactions between endogenous and exogenous attention on cortical visual processing. NeuroImage 2006, 31:774-789.
32. Key A.P.F., Dove G.O., Maguire M.J. Linking brainwaves to the brain: an ERP primer. Dev. Neuropsychol. 2005, 27(2):183-215.
33. Laurens K.R., Kiehl K.A., Liddle P.F. A supramodal limbic-paralimbic-neocortical network supports goal-directed stimulus processing. Hum. Brain Mapp. 2005, 24(1):35-49.
34. Linden D.E.J. The P300: where in the brain is it produced and what does it tell us?. Neuroscientist 2005, 11:563-576.
35. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453(7197):869-878.
36. Luck S.J., Woodman G.E., Vogel E.K. Event-related potential studies of attention. Trends Cogn. Sci. 2000, 4:432-440.
37. MacDonald A.W., Cohen J.D., Stenger V.A., Carter C.S. Dissociating the role of the dorsolateral prefrontal cortex in cognitive control. Science 2000, 288(5472):1835-1838.
38. Makeig S., Westerfield M., Jung T.-P., Covington J., Townsend J., Sejnowski T.J., Courschesne E. Functionally independent components of the late positive event-related potential during visual spatial attention. J. Neurosci. 1999, 19(7):2665-2680.
39. Makeig S., Delorme A., Westerfield M., Jung T.-P., Townsend J., Courschesne E., Sejnowski T.J. Electroencephalographic brain dynamics following manually responded visual targets. PLoS Biol. 2004, 2(6):747-762.
40. Mantini D., Perrucci M.G., Del Gratta C., Romani G.L., Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(32):13170-13175.
41. Mattle H., Edelman R.R., Reis M.A., Atkinson D.J. Flow quantification in the superior sagittal sinus using magnetic resonance. Neurology 1990, 40(5):813.
42. Mukamel R., Gelbard H., Arieli A., Hasson U., Fried I., Malach R. Coupling between neuronal firing, field potentials, and fMRI in human auditory cortex. Science 2005, 309:951-954.
43. Mulert C., Seifert C., Leicht G., Kirsch V., Ertl M., Karch S., Moosmann M., Lutz J., Möller H.-J., Hegerl U., Pogarell O., Jäger L. Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making. NeuroImage 2008, 42:158-168.
44. Murray S.O., Wojciulik E. Attention increases neural selectivity in the human lateral occipital complex. Nat. Neurosci. 2003, 7(1):70-74.
45. Nieuwenhuis S., Aston-Jones G., Cohen J.D. Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychol. Bull. 2005, 131(4):510-532.
46. Novitskiy N., Ramautar J.R., Vanderperren K., De Vos M., Mennes M., Mijovic B., Vanrumste B., Stiers P., Van den Bergh B., Lagae L., Sunaert S., Van Huffel S., Wagemans J. The BOLD correlates of the visual P1 and N1 in single-trial analysis of simultaneous EEG-fMRI recordings during a spatial detection task. NeuroImage 2011, 54:824-835.
47. Ossandon T., Jerbi K., Vidal J.R., Bayle D.J., Henaff M.-A., Jung J., Minotti L., Bertrand O., Kahane P., Lachaux J.-P. Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance. J. Neurosci. 2011, 31(41):14521-14530.
48. Palva J.M., Palva S. Infra-slow fluctuations in electrophysiological recordings, blood-oxygenation-level-dependent signals, and psychophysical time series. NeuroImage 2012, 62:2201-2211.
49. Parra L.C., Alvino C., Tang A., Pearlmutter B., Young N., Osman A., Sajda P. Linear spatial integration for single-trial detection in encephalography. NeuroImage 2002, 17:223-230.
50. Parra L.C., Spence C.D., Gerson A.D., Sajda P. Recipes for the linear analysis of EEG. NeuroImage 2005, 28(2):342-353.
51. Philiastides M.G., Ratcliff R., Sajda P. Neural representation of task difficulty and decision making during perceptual categorization: a timing diagram. J. Neurosci. 2007, 26(35):8965-8975.
52. Polich J. Updating P300: an integrative theory of P3a and P3b. Clin. Neurophysiol. 2007, 118:2128-2148.
53. 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.
54. Sajda P., Goldman R.I., Dyrholm M., Brown T.R. Chapter 9: signal processing and machine learning for single-trial analysis of simultaneously acquired EEG and fMRI. Statistical Signal Processing for Neuroscience and Neurotechnology 2010, Academic Press. K.G. Oweiss (Ed.).
55. Scheeringa R., Bastiaansen M.C.M., Petersson K.M., Oostenveld R., Norris D.G., Hagoort P. Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int. J. Psychophysiol. 2008, 67(3):242-251.
56. Scheeringa R., Fries P., Petersson K.M., Oostenveld R., Grothe I., Norris D.G., Hagoort P., Bastiaansen M.C.M. Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 2011, 69:572-583.
57. Scheibe C., Ullsperger M., Sommer W., Heekeren H.R. Effects of parametrical and trial-to-trial variation in prior probability processing revealed by simultaneous electroencephalogram/functional magnetic resonance imaging. J. Neurosci. 2010, 30(49):16709-16717.
58. Schooler J.W. Introspecting in the spirit of William James: comment on Fox, Ericsson, and Best (2011). Psychol. Bull. 2011, 137(2):345-350.
59. Singh K.D., Fawcett I.P. Transient and linearly graded deactivation of the human default-mode network by a visual detection task. NeuroImage 2008, 41:100-112.
60. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44(1):83-98.
61. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
62. Stevens A.A., Skudlarski P., Gatenby J., Gore J.C. Event-related fMRI of auditory and visual oddball tasks. Magn. Reson Imaging 2000, 18:495-502.
63. Stoodley C.J., Schmahmann J.D. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage 2009, 44(2):489-501.
64. Stoodley C.J., Valera E.M., Schmahmann J.D. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. NeuroImage 2012, 59(2):1560-1570.
65. Strang G. Chapter 4: orthogonality. Introduction to Linear Algebra 2003, Wellesley-Cambridge Press, Wellesley, MA. 3rd ed.
66. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 2009, 30(9):2731-2745.
67. Udin L.Q., Supekar K., Amin H., Rykhlevskaia E., Nguyen D.A., Greicius M.D., Menon V. Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb. Cortex 2010, 20(11):2636-2646.
68. Vanhaudenhuyse A., Demertzi A., Schabus M., Noirhomme Q., Bredart S., Boly M., Phillips C., Soddu A., Luxen A., Moonen G., Laureys S. Two distinct neuronal networks mediate the awareness of environment and of self. J. Cogn. Neurosci. 2011, 23(3):570-578.
69. Warbrick T., Mobascher A., Brinkmeyer J., Musso F., Richter N., Stoecker T., Fink G.R., Shah N.J., Winterer G. Single-trial P3 amplitude and latency informed event-related fMRI models yield different BOLD response patterns to a target detection task. NeuroImage 2009, 47:1532-1544.
70. Weissman D.H., Roberts K.C., Visscher K.M., Woldorff M.G. The neural bases of momentary lapses in attention. Nat. Neurosci. 2006, 9:971-978.
71. Worsley K.J. Chapter 14: statistical analysis of activation images. Functional MRI: An Introduction to Methods 2001, Oxford University Press. P. Jezzard, P.M. Matthews, S.M. Smith (Eds.).
72. Yarkoni T., Barch D.M., Gray J.R., Conturo T.E., Braver T.S. BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis. PLoS One 2009, 4(1):e4257.
73. Yarkoni T., Poldrack R.A., Nichols T.E., Van Essen D.C., Wager T.D. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 2011, 8:665-670.