Ongoing EEG phase as a trial-by-trial predictor of perceptual and attentional variability

Frontiers in Psychology

Volumn 2, Issue APR, 2011, Pages

  VanRullen, R ^a,b   Busch, N A ^c,d   Drewes, J ^a,b   Dubois, Julien ^a,b,e  

^a Brain and Cognition Research Center in Toulouse   (France)

^b CNRS   (France)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Attention; EEG; Ongoing; Oscillation; Perception; Phase; Pre stimulus; Spontaneous

Indexed keywords

EID: 84859110415     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2011.00060     Document Type: Article

References (98)

1. Allport, D. A. (1968). Phenomenal simutaneity and the perceptual moment hypothesis. Br. J. Psychol. 59, 395-406.
2. Alvarez, G. A., and Cavanagh, P. (2004). The capacity of visual short-term memory is set both by visual information load and by number of objects. Psychol. Sci. 15, 106-111.
3. Andrews, T., and Purves, D. (2005). The wagon-wheel illusion in continuous light. Trends Cogn. Sci. (Regul. Ed.) 9, 261-263.
4. Andrews, T., Purves, D., Simpson, W. A., and VanRullen, R. (2005). The wheel keeps turning: reply to Holcombe et al. Trends Cogn. Sci. (Regul. Ed.) 9, 561.
5. Awh, E., Anllo-Vento, L., and Hillyard, S. A. (2000). The role of spatial selective attention in working memory for locations: evidence from eventrelated potentials. J. Cogn. Neurosci. 12, 840-847.
6. Awh, E., and Jonides, J. (2001). Overlapping mechanisms of attention and spatial working memory. Trends Cogn. Sci. (Regul. Ed.) 5, 119-126.
7. Awh, E., Vogel, E. K., and Oh, S. H. (2006). Interactions between attention and working memory. Neuroscience 139, 201-208.
8. Berens, P. (2009). CircStat: a MATLAB Toolbox for circular statistics. J. Stat. Softw. 31, 1-21.
9. Bestmann, S., Ruff, C. C., Blakemore, C., Driver, J., and Thilo, K. V. (2007). Spatial attention changes excitability of human visual cortex to direct stimulation. Curr. Biol. 17, 134-139.
10. Brandt, M. E. (1997). Visual and auditory evoked phase resetting of the alpha EEG. Int. J. Psychophysiol. 26, 285-298.
11. Busch, N. A., Dubois, J., and VanRullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. J. Neurosci. 29, 7869-7876.
12. Busch, N. A., and VanRullen, R. (2010). Spontaneous EEG oscillations reveal periodic sampling of visual attention. Proc. Natl. Acad. Sci. U.S.A. 107, 16048-16053.
13. Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340.
14. Buzsaki, G. (2006). Rhythms of the Brain. New York: Oxford University Press.
15. Callaway, E. I., and Yeager, C. L. (1960). Relationship between reaction time and electroencephalographic alpha phase. Science 132, 1765-1766.
16. Calvin, W. H., and Stevens, C. F. (1967). Synaptic noise as a source of variability in the interval between action potentials. Science 155, 842-844.
17. Carlson, T. A., Hogendoorn, H., and Verstraten, F. A. (2006). The speed of visual attention: what time is it? J. Vis. 6, 1406-1411.
18. Corbetta, M., and Shulman, G. L. (1998). Human cortical mechanisms of visual attention during orienting and search. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1353-1362.
19. Cowan, N. (2001). The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav. Brain Sci. 24, 87-114.
20. Crowne, D. P. (1983). The frontal eye field and attention. Psychol. Bull. 93, 232-260.
21. de Fockert, J. W., Rees, G., Frith, C. D., and Lavie, N. (2001). The role of working memory in visual selective attention. Science 291, 1803-1806.
22. Desgranges, B., Baron, J. C., and Eustache, F. (1998). The functional neuroanatomy of episodic memory: the role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage 8, 198-213.
23. Deubel, H., and Schneider, W. X. (1996). Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Res. 36, 1827-1837.
24. Downing, P. E. (2000). Interactions between visual working memory and selective attention. Psychol. Sci. 11, 467-473.
25. Drewes, J., and VanRullen, R. (2011). This is the rhythm of your eyes: the phase of ongoing EEG oscillations modulates saccadic reaction time. J. Neurosci. 31, 4698-4708.
26. Dustman, R. E., and Beck, E. C. (1965). Phase of alpha brain waves, reaction time and visually evoked potentials. Electroencephalogr. Clin. Neurophysiol. 18, 433-440.
27. Engel, A. K., and Singer, W. (2001). Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. (Regul. Ed.) 5, 16-25.
28. Ergenoglu, T., Demiralp, T., Bayraktaroglu, Z., Ergen, M., Beydagi, H., and Uresin, Y. (2004). Alpha rhythm of the EEG modulates visual detection performance in humans. Brain Res. Cogn. Brain Res. 20, 376-383.
29. Fischer, B., and Boch, R. (1983). Saccadic eye movements after extremely short reaction times in the monkey. Brain Res. 260, 21-26.
30. Fischer, B., and Ramsperger, E. (1984). Human express saccades: extremely short reaction times of goal directed eye movements. Exp. Brain Res. 57, 191-195.
31. Fries, P., Neuenschwander, S., Engel, A. K., Goebel, R., and Singer, W. (2001). Rapid feature selective neuronal synchronization through correlated latency shifting. Nat. Neurosci. 4, 194-200.
32. Fries, P., Nikolic, D., and Singer, W. (2007). The gamma cycle. Trends Neurosci. 30, 309-316.
33. Gho, M., and Varela, F. J. (1988). A quantitative assessment of the dependency of the visual temporal frame upon the cortical rhythm. J. Physiol. 83, 95-101.
34. Hanslmayr, S., Aslan, A., Staudigl, T., Klimesch, W., Herrmann, C. S., and Bauml, K. H. (2007). Prestimulus oscillations predict visual perception performance between and within subjects. Neuroimage 37, 1465-1473.
35. Hanslmayr, S., Klimesch, W., Sauseng, P., Gruber, W., Doppelmayr, M., Freunberger, R., and Pecherstorfer, T. (2005). Visual discrimination performance is related to decreased alpha amplitude but increased phase locking. Neurosci. Lett. 375, 64-68.
36. Harter, M. R. (1967). Excitability cycles and cortical scanning: a review of two hypotheses of central intermittency in perception. Psychol. Bull. 68, 47-58.
37. Holcombe, A. O., Clifford, C. W., Eagleman, D. M., and Pakarian, P. (2005). Illusory motion reversal in tune with motion detectors. Trends Cogn. Sci. (Regul. Ed.) 9, 559-560.
38. Ilmoniemi, R. J., and Kicic, D. (2010). Methodology for combined TMS and EEG. Brain Topogr. 22, 233-248.
39. Jansen, B. H., and Brandt, M. E. (1991). The effect of the phase of prestimulus alpha activity on the averaged visual evoked response. Electroencephalogr. Clin. Neurophysiol. 80, 241-250.
40. Jones, M. W., and Wilson, M. A. (2005). Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15, 867-873.
41. Juan, C. H., Shorter-Jacobi, S. M., and Schall, J. D. (2004). Dissociation of spatial attention and saccade preparation. Proc. Natl. Acad. Sci. U.S.A. 101, 15541-15544.
42. Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Brain Res. Rev. 29, 169-195.
43. Kline, K., and Eagleman, D. M. (2008). Evidence against the temporal subsampling account of illusory motion reversal. J. Vis. 8, 13.1-13.5.
44. Kline, K., Holcombe, A. O., and Eagleman, D. M. (2004). Illusory motion reversal is caused by rivalry, not by perceptual snapshots of the visual field. Vision Res. 44, 2653-2658.
45. Kodaka, Y., Mikami, A., and Kubota, K. (1997). Neuronal activity in the frontal eye field of the monkey is modulated while attention is focused on to a stimulus in the peripheral visual field, irrespective of eye movement. Neurosci. Res. 28, 291-298.
46. Kramer, J. H., Rosen, H. J., Du, A. T., Schuff, N., Hollnagel, C., Weiner, M. W., Miller, B. L., and Delis, D. C. (2005). Dissociations in hippocampal and frontal contributions to episodic memory performance. Neuropsychology 19, 799-805.
47. Kruglikov, S. Y., and Schiff, S. J. (2003). Interplay of electroencephalogram phase and auditory-evoked neural activity. J. Neurosci. 23, 10122-10127.
48. LaBar, K. S., Gitelman, D. R., Parrish, T. B., and Mesulam, M. (1999). Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects. Neuroimage 10, 695-704.
49. Lachaux, J. P., Rodriguez, E., Martinerie, J., and Varela, F. J. (1999). Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194-208.
50. Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., and Schroeder, C. E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110-113.
51. Lakatos, P., O'Connell, M. N., Barczak, A., Mills, A., Javitt, D. C., and Schroeder, C. E. (2009). The leading sense: supramodal control of neurophysiological context by attention. Neuron 64, 419-430.
52. Lansing, R. W. (1957). Relation of brain and tremor rhythms to visual reaction time. Electroencephalogr. Clin. Neurophysiol. 9, 497-504.
53. Large, E. W., and Jones, M. R. (1999). The dynamics of attending: how people track time-varying events. Psychol. Rev. 106, 119-159.
54. Levitan, H., Segundo, J. P., Moore, G. P., and Perkel, D. H. (1968). Statistical analysis of membrane potential fluctuations. Relation with presynaptic spike train. Biophys. J. 8, 1256-1274.
55. Lisman, J. E., and Idiart, M. A. (1995). Storage of 7±2 short-term memories in oscillatory subcycles. Science 267, 1512-1515.
56. Luck, S. J., and Vogel, E. K. (1997). The capacity of visual working memory for features and conjunctions. Nature 390, 279-281.
57. Mathewson, K. E., Fabiani, M., Gratton, G., Beck, D. M., and Lleras, A. (2010). Rescuing stimuli from invisibility: inducing a momentary release from visual masking with pre-target entrainment. Cognition 115, 186-191.
58. Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M., and Ro, T. (2009). To see or not to see: prestimulus alpha phase predicts visual awareness. J. Neurosci. 29, 2725-2732.
59. Montemurro, M. A., Rasch, M. J., Murayama, Y., Logothetis, N. K., and Panzeri, S. (2008). Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr. Biol. 18, 375-380.
60. Moore, T., and Fallah, M. (2001). Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. U.S.A. 98, 1273-1276.
61. Murthy, A., Thompson, K. G., and Schall, J. D. (2001). Dynamic dissociation of visual selection from saccade programming in frontal eye field. J. Neurophysiol. 86, 2634-2637.
62. O'Keefe, J. (1993). Hippocampus, theta, and spatial memory. Curr. Opin. Neurobiol. 3, 917-924.
63. O'Keefe, J., and Recce, M. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330.
64. Pitts, W., and McCulloch, W. S. (1947). How we know universals: the perception of auditory and visual forms. Bull. Math. Biophys. 9, 127-147.
65. Poldrack, R. A., and Gabrieli, J. D. (1997). Functional anatomy of long-term memory. J. Clin. Neurophysiol. 14, 294-310.
66. Purves, D., Paydarfar, J. A., and Andrews, T. J. (1996). The wagon wheel illusion in movies and reality. Proc. Natl. Acad. Sci. U.S.A. 93, 3693-3697.
67. Ramus, S. J., Davis, J. B., Donahue, R. J., Discenza, C. B., and Waite, A. A. (2007). Interactions between the orbitofrontal cortex and the hippocampal memory system during the storage of long-term memory. Ann. N. Y. Acad. Sci. 1121, 216-231.
68. Rizzolatti, G., Riggio, L., Dascola, I., and Umilta, C. (1987). Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25, 31-40.
69. Rutishauser, U., Ross, I. B., Mamelak, A. N., and Schuman, E. M. (2010). Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903-907.
70. Schall, J. D. (2004). On the role of frontal eye field in guiding attention and saccades. Vision Res. 44, 1453-1467.
71. Schroeder, C. E., and Lakatos, P. (2009). Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 32, 9-18.
72. Siapas, A. G., Lubenov, E. V., and Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151.
73. Siegel, M., Warden, M. R., and Miller, E. K. (2009). Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl. Acad. Sci. U.S.A. 106, 21341-21346.
74. Skaggs, W. E., McNaughton, B. L., Wilson, M. A., and Barnes, C. A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172.
75. Smith, D. T., Rorden, C., and Jackson, S. R. (2004). Exogenous orienting of attention depends upon the ability to execute eye movements. Curr. Biol. 14, 792-795.
76. Stern, E. A., Kincaid, A. E., and Wilson, C. J. (1997). Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697-1715.
77. Sternberg, S. (1966). High-speed scanning in human memory. Science 153, 652-654.
78. Stroud, J. M. (1956). "The fine structure of psychological time," in Information Theory in Psychology, ed. H. Quastler (Chicago, IL: Free Press) 174-205.
79. Tallon-Baudry, C., and Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. (Regul. Ed.) 3, 151-162
80. Taylor, P. C., Walsh, V., and Eimer, M. (2008). Combining TMS and EEG to study cognitive function and corticocortico interactions. Behav. Brain Res. 191, 141-147.
81. Thut, G., Ives, J. R., Kampmann, F., Pastor, M. A., and Pascual-Leone, A. (2005). A new device and protocol for combining TMS and online recordings of EEG and evoked potentials. J. Neurosci. Methods 141, 207-217.
82. Thut, G., and Miniussi, C. (2009). New insights into rhythmic brain activity from TMS-EEG studies. Trends Cogn. Sci. (Regul. Ed.) 13, 182-189.
83. Thut, G., Nietzel, A., Brandt, S. A., and Pascual-Leone, A. (2006). Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J. Neurosci. 26, 9494-9502.
84. Thut, G., and Pascual-Leone, A. (2010). Integrating TMS with EEG: how and what for? Brain Topogr. 22, 215-218.
85. van Dijk, H., Schoffelen, J. M., Oostenveld, R., and Jensen, O. (2008). Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J. Neurosci. 28, 1816-1823.
86. VanRullen, R., Carlson, T., and Cavanagh, P. (2007). The blinking spotlight of attention. Proc. Natl. Acad. Sci. U.S.A. 104, 19204-19209.
87. VanRullen, R., Guyonneau, R., and Thorpe, S. J. (2005a). Spike times make sense. Trends Neurosci. 28, 1-4.
88. VanRullen, R., Reddy, L., and Koch, C. (2005b). Attention-driven discrete sampling of motion perception. Proc. Natl. Acad. Sci. U.S.A. 102, 5291-5296.
89. VanRullen, R., and Koch, C. (2003). Is perception discrete or continuous? Trends Cogn. Sci. (Regul. Ed.) 7, 207-213.
90. VanRullen, R., Reddy, L., and Koch, C. (2006). The continuous wagon wheel illusion is associated with changes in electroencephalogram power at approximately 13 Hz. J. Neurosci. 26, 502-507
91. Varela, F., Lachaux, J. P., Rodriguez, E., and Martinerie, J. (2001). The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229-239.
92. Varela, F. J., Toro, A., John, E. R., and Schwartz, E. L. (1981). Perceptual framing and cortical alpha rhythm. Neuropsychologia 19, 675-686.
93. Vinck, M., Lima, B., Womelsdorf, T., Oostenveld, R., Singer, W., Neuenschwander, S., and Fries, P. (2010a). Gamma-phase shifting in awake monkey visual cortex. J. Neurosci. 30, 1250-1257.
94. Vinck, M., van Wingerden, M., Womelsdorf, T., Fries, P., and Pennartz, C. M. (2010b). The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. Neuroimage 51, 112-122.
95. Walsh, E. G. (1952). Visual reaction time and the alpha-rhythm, an investigation of a scanning hypothesis. J. Physiol. 118, 500-508.
96. Wardak, C., Ibos, G., Duhamel, J. R., and Olivier, E. (2006). Contribution of the monkey frontal eye field to covert visual attention. J. Neurosci. 26, 4228-4235.
97. Woodman, G. F., Luck, S. J., and Schall, J. D. (2007). The role of working memory representations in the control of attention. Cereb. Cortex 17(Suppl. 1), i118-i124.
98. Woodman, G. F., Vogel, E. K., and Luck, S. J. (2001). Visual search remains efficient when visual working memory is full. Psychol. Sci. 12, 219-224.