In the blink of an eye: The contribution of microsaccadic activity to the induced gamma band response

International Journal of Psychophysiology

Volumn 79, Issue 1, 2011, Pages 73-82

  Schwartzman, David J ^a   Kranczioch, Cornelia ^b  

^a OXFORD BROOKES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

EEG; ICA; Induced gamma band response; Microsaccade; Saccadic spike potential

Indexed keywords

ELECTROENCEPHALOGRAM; EVOKED CORTICAL RESPONSE; EXTRAOCULAR MUSCLE; HUMAN; INDUCED GAMMA BAND RESPONSE; MICROSACCADE; NONHUMAN; REVIEW; SCALP; SPIKE WAVE; VISUAL STIMULATION;

ANIMALS; BLINKING; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; EYE; HUMANS; PHOTIC STIMULATION; SACCADES; TIME FACTORS;

EID: 79251621406     PISSN: 01678760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpsycho.2010.10.006     Document Type: Review

References (92)

1. Anaki D., Zion-Golumbic E., Bentin S. Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces. Neuroimage 2007, 37:1407-1416.
2. Armington J.C., Bloom M.B. Relations between the amplitudes of spontaneous saccades and visual responses. J. Opt. Soc. Am. 1974, 64:1263-1271.
3. Aru J., Bachmann T. Occipital EEG correlates of conscious awareness when subjective target shine-through and effective visual masking are compared: bifocal early increase in gamma power and speed-up of P1. Brain Res. 2009, 1271:60-73.
4. Busch N.A., Herrmann C.S., Muller M.M., Lenz D., Gruber T. A cross-laboratory study of event-related gamma activity in a standard object recognition paradigm. Neuroimage 2006, 33:1169-1177.
5. 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.
6. Croft R.J., Barry R.J. Removal of ocular artifact from the EEG: a review. Neurophysiol. Clin. 2000, 30:5-19.
7. Croft R.J., Chandler J.S., Barry R.J., Cooper N.R., Clarke A.R. EOG correction: a comparison of four methods. Psychophysiology 2005, 42:16-24.
8. Debener S., Hine J., Bleeck S., Eyles J. Source localization of auditory evoked potentials after cochlear implantation. Psychophysiology 2008, 45:20-24.
9. Debener S., Mullinger K.J., Niazy R.K., Bowtell R.W. Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. Int. J. Psychophysiol. 2008, 67:189-199.
10. Debener S., Thorne J., Schneider T.R., Viola F.C. Using ICA for the analysis of multi-channel EEG Data. Recording, Analysis and Application 2010, 121-134. Oxford University Press, Oxford. D. Debener, M. Ullsperger (Eds.).
11. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 2004, 134:9-211.
12. Dimigen O., Valsecchi M., Sommer W., Kliegl R. Human microsaccade-related visual brain responses. J. Neurosci. 2009, 29:12321-12331.
13. Eckhorn R., Bauer R., Jordan W., Brosch M., Kruse W., Munk M., Reitboeck H.J. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol. Cybern. 1988, 60:121-130.
14. Engbert R. Flick-induced flips in perception. Neuron 2006, 49:168-170.
15. Engbert R. Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception. Prog. Brain Res. 2006, 154:177-192.
16. Engbert R., Kliegl R. Microsaccades uncover the orientation of covert attention. Vis. Res. 2003, 43:1035-1045.
17. Fries P., Scheeringa R., Oostenveld R. Finding gamma. Neuron 2008, 58:303-305.
18. Gasser T., Sroka L., Mocks J. The transfer of EOG activity into the EEG for eyes open and closed. Electroencephalogr. Clin. Neurophysiol. 1985, 61:181-193.
19. Gratton G., Coles M.G., Donchin E. A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 1983, 55:468-484.
20. Gray C.M., Konig P., Engel A.K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 1989, 338:334-347.
21. Gruber T., Muller M.M., Keil A., Elbert T. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin. Neurophysiol. 1999, 110:2074-2085.
22. Gruber T., Müller M.M., Keil A., Elbert T. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin. Neurophysiol. 1999, 110:2074-2085.
23. Gruber T., Müller M.M., Keil A. Modulation of induced gamma band responses in a perceptual learning task in the human EEG. J. Cogn. Neurosci. 2002, 14:732-744.
24. Gruber T., Malinowski P., Müller M.M. Modulation of oscillatory brain activity and evoked potentials in a repetition priming task in the human EEG. Eur. J. Neurosci. 2004, 19:1073-1082.
25. Gruber T., Maess B., Trujillo-Barreto N.J., Müller M.M. Sources of synchronized induced Gamma-Band responses during a simple object recognition task: a replication study in human MEG. Brain Res. 2008, 1196:74-84.
26. Gruber T., Martinovic J., Müller M.M. It's all in your eyes? Induced gamma band responses in human EEG. Neuron 2008, 58. on-line reply http://www.cell.com/neuron/viewComment/S0896-6273%2808%2900301-2 [Accessed 25 July 2010].
27. Gruber T., Martinovic J., Müller M.M. It's all in your eyes? Induced gamma band responses in the human EEG. Supplementary figures to our reply to Yuval-Greenberg et al. (2008, Neuron) 2008, [Online] Available at: http://www.uni-leipzig.de/~psyall2/download/SP_infos/SP_infos.pdf [Accessed 25 July 2010].
28. Hauk O., Keil A., Elbert T., Müller M.M. Comparison of data transformation procedures to enhance topographical accuracy in time-series analysis of the human EEG. J. Neurosci. Methods 2002, 113:111-122.
29. Herrmann C.S., Lenz D., Junge S., Busch N.A., Maess B. Memory-matches evoke human gamma-responses. BMC Neurosci. 2004, 5:13-21.
30. Herrmann C.S., Fründ I., Lenz D. Human gamma-band activity: a review on cognitive and behavioral correlates and network models. Neurosci. Biobehav. Rev. 2010, 34:981-992.
31. Hine J., Debener S. Late auditory evoked potentials asymmetry revisited. Clin. Neurophysiol. 2007, 118:1274-1285.
32. Hjorth B. An on-line transformation of EEG scalp potentials into orthogonal source. Electroencephalogr. Clin. Neurophysiol. 1975, 39(5):526-530.
33. Hoffmann S., Falkenstein M. The correction of eye blink artefacts in the EEG: a comparison of two prominent methods. PLoS ONE 2008, 3:e3004.
34. Hoogenboom N., Schoffelen J.M., Oostenveld R., Parkes L.M., Fries P. Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 2006, 29:764-773.
35. Horowitz T.S., Fine E.M., Fencsik D.E., Yurgenson S., Wolfe J.M. Fixational eye movements are not an index of covert attention. Psychol. Sci. 2007, 18:356-363.
36. Jerbi, K., Freyermuth, S., Dalal, S., Kahane, P., Bertrand, O., Berthoz, A., Lachaux, J., 2009. Saccade related gamma-band activity in intracerebral EEG: dissociating neural from ocular muscle activity. Brain Topog. 22, 18-23.
37. Juergens E., Guettler A., Eckhorn R. Visual stimulation elicits locked and induced gamma oscillations in monkey intracortical- and EEG-potentials, but not in human EEG. Exp. Brain Res. 1999, 129:247-259.
38. Jung T.P., Makeig S., Humphries C., Lee T.W., Mckeown M.J., Iragui V., Sejnowski T.J. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000, 37:163-178.
39. Jung T.P., Makeig S., Westerfield M., Townsend J., Courchesne E., Sejnowski T.J. Analysis and visualization of single-trial event-related potentials. Hum. Brain Mapp. 2001, 14:166-185.
40. Jutras M.J., Buffalo E.A. Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 2010, 20:150-155.
41. Kaiser J., Lutzenberger W., Decker C., Wibral M., Rahm B. Task- and performance-related modulation of domain-specific auditory short-term memory representations in the gamma-band. Neuroimage 2009, 46:1127-1136.
42. Katila T., Maniewski R., Poutanen T., Varpula T., Karp P.J. Magnetic-fields produced by the human-eye. J. Appl. Phys. 1981, 52:2565-2571.
43. Keren A.S., Yuval-Greenberg S., Deouell L.Y. Saccadic spike potentials in gamma-band EEG: characterization, detection and suppression. Neuroimage 2010, 49:2248-2263.
44. Kowler E., Steinman R.M. Small saccades serve no useful purpose: reply to a letter by R. W. Ditchburn. Vis. Res. 1980, 20:273-276.
45. Kranczioch C., Debener S., Herrmann C.S., Engel A.K. EEG gamma-band activity in rapid serial visual presentation. Exp. Brain Res. 2005, 169:246-254.
46. Kranczioch C., Debener S., Maye A., Engel A.K. Temporal dynamics of access to consciousness in the attentional blink. Neuroimage 2007, 37:947-955.
47. Lee S., Kim D., Kim E., Kim S., Im C. Dysfunctional gamma-band activity during face structural processing in schizophrenia patients. Schizo. Research 2010, 119:191-197.
48. Leopold D.A., Logothetis N.K. Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp. Brain Res. 1998, 123:341-345.
49. Li Y., Ma Z., Lu W., Li Y. Automatic removal of the eye blink artifact from EEG using an ICA-based template matching approach. Physiol. Meas. 2006, 27:425-436.
50. Lutzenberger W., Pulvermüller F., Birbaumer N. Words and pseudowords elicit distinct patterns of 30-Hz EEG responses in humans. Neurosci. Lett. 1994, 176:115-118.
51. Lutzenberger W., Pulvermüller F., Elbert T., Birbaumer N. Visual stimulation alters local 40-Hz responses in humans: an EEG-study. Neurosci. Lett. 1995, 183:39-42.
52. Makeig S., Jung T.P., Bell A.J., Ghahremani D., Sejnowski T.J. Blind separation of auditory event-related brain responses into independent components. Proc. Natl Acad. Sci. USA 1997, 94:10979-10984.
53. Martinez-Conde S., Macknik S.L., Hubel D.H. The role of fixational eye movements in visual perception. Nat. Rev. Neurosci. 2004, 5:229-240.
54. Martinez-Conde S., Macknik S.L., Troncoso X.G., Dyar T.A. Microsaccades counteract visual fading during fixation. Neuron 2006, 49:297-305.
55. Melloni L., Schwiedrzik C.M., Rodriguez E., Singer W. (Micro)Saccades, corollary activity and cortical oscillations. Trends Cogn. Sci. 2009, 13:239-245.
56. Melloni L., Schwiedrzik C.M., Wibral M., Rodriguez E., Singer W. Response to: Yuval-Greenberg et al., "Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades". Neuron 2009, 58:429-441.
57. Mognon, A., Jovicich, J., Bruzzone, L., Buiatti, M., in press. ADJUST: An Automatic EEG artifact Detector based on the Joint Use of Spatial and Temporal features. Psychophysiology. Available at http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8986.2010.01061.x/full.
58. Moldakarimov S., Bazhenov M., Sejnowski T.J. Perceptual priming leads to reduction of gamma frequency oscillations. Proc. Natl Acad. Sci. USA 2010, 12:5640-5645.
59. Müller M.M., Gruber T., Keil A. Modulation of induced gamma band activity in the human EEG by attention and visual information processing. Int. J. Psychophysiol. 2000, 38:283-299.
60. Nottage J.F. Uncovering gamma in visual tasks. Brain Topogr. 2010, 23:58-71.
61. Onton J., Westerfield M., Townsend J., Makeig S. Imaging human EEG dynamics using independent component analysis. Neurosci. Biobehav. Rev. 2006, 30:808-822.
62. Pope K.J., Fitzgibbon S.P., Lewis T.W., Whitham E.M., Willoughby J.O. Relation of gamma oscillations in scalp recordings to muscular activity. Brain Topogr. 2009, 22:13-17.
63. Pulvermüller F., Lutzenberger W., Preissl H. Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. Cereb. Cortex 1999, 9:497-506.
64. Reppas J.B., Usrey W.M., Reid R.C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 2002, 35:961-974.
65. Reva N.V., Aftanas L.I. The coincidence between late non-phase-locked gamma synchronization response and saccadic eye movements. Int. J. Psychophysiol. 2004, 51:215-222.
66. Rolfs M. Microsaccades: small steps on a long way. Vis. Res. 2009, 49:2415-2441.
67. Rolfs M., Kliegl R., Engbert R. Toward a model of microsaccade generation: the case of microsaccadic inhibition. J. Vis. 2008, 8(5):1-23.
68. Schneider T.R., Debener S., Oostenveld R., Engel A.K. Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming. Neuroimage 2008, 42:1244-1254.
69. Schwind J., Dormann W.U. Off-line removal of ocular artifacts from event-related potentials using a multiple linear regression model. Int. J. Psychophysiol. 1986, 4:203-208.
70. Semlitsch H.V., Anderer P., Schuster P., Presslich O. A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology 1986, 23:695-703.
71. Shackman A.J., Mcmenamin B.W., Slagter H.A., Maxwell J.S., Greischar L.L., Davidson R.J. Electromyogenic artifacts and electroencephalographic inferences. Brain Topogr. 2009, 22:7-12.
72. Shackman A.J., Mcmenamin B.W., Maxwell J.S., Greischar L.L., Davidson R.J. Identifying robust and sensitive frequency bands for interrogating neural oscillations. Neuroimage 2010, 51:1319-1333.
73. Skavenski A.A., Hansen R.M., Steinman R.M., Winterson B.J. Quality of retinal image stabilization during small natural and artificial body rotations in man. Vis. Res. 1979, 19:675-683.
74. Steinman R.M., Cunitz R.J., Timberlake G.T., Herman M. Voluntary control of microsaccades during maintained monocular fixation. Science 1967, 155:1577-1579.
75. Tallon-Baudry C. Do not throw out the baby with the bath water: induced gamma-band oscillations can be detected in scalp EEG data. Neuron 2008, 58. on-line reply http://www.cell.com/neuron/viewComment/S0896-6273%2808%2900301-2 accessed 25 July 2010.
76. Tallon-Baudry C. The roles of gamma-band oscillatory synchrony in human visual cognition. Front. Biosci. 2009, 14:321-332.
77. Tallon-Baudry C., Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 1999, 3:151-162.
78. Tallon-Baudry C., Bertrand O., Delpuech C., Pernier J. Stimulus specificity of phase-locked and non-phase-locked 40Hz visual responses in human. J. Neurosci. 1996, 16:4240-4249.
79. Tallon-Baudry C., Bertrand O., Delpuech C., Permier J. Oscillatory gamma-band (30-70Hz) activity induced by a visual search task in humans. J. Neurosci. 1997, 17:722-734.
80. Tallon-Baudry C., Bertrand O., Peronnet F., Pernier J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 1998, 18:4244-4254.
81. Tallon-Baudry C., Bertrand O., Hénaff M., Isnard J., Fischer C. Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb. Cortex. 2005, 15(5):654-662.
82. Thickbroom G.W., Mastaglia F.L. Presaccadic 'spike' potential: investigation of topography and source. Brain Res. 1985, 339:271-280.
83. Thickbroom G.W., Mastaglia F.L. Presaccadic spike potential. Relation to eye movement direction. Electroencephalogr. Clin. Neurophysiol. 1986, 64:211-214.
84. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 2010, 11:100-113.
85. Valsecchi M., Turatto M. Microsaccadic response to visual events that are invisible to the superior colliculus. Behav. Neurosci. 2007, 121:786-793.
86. Valsecchi M., Turatto M. Microsaccadic responses in a bimodal oddball task. Psychol. Res. 2009, 73:23-33.
87. Viola F.C., Thorne J., Edmonds B., Schneider T., Eichele T., Debener S. Semi-automatic identification of independent components representing EEG artifact. Clin. Neurophysiol. 2009, 120:868-877.
88. Yeung N., Bogacz R., Holroyd C.B., Cohen J.D. Detection of synchronized oscillations in the electroencephalogram: an evaluation of methods. Psychophysiology 2004, 41:822-832.
89. Yuval-Greenberg S., Deouell L.Y. The broadband-transient induced gamma-band response in scalp EEG reflects the execution of saccades. Brain Topogr. 2009, 22:3-6.
90. Yuval-Greenberg S., Tomer O., Keren A.S., Nelken I., Deouell L.Y. Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron 2008, 58:429-441.
91. Zion-Golumbic E., Bentin S. Dissociated neural mechanisms for face detection and configural encoding: evidence from N170 and induced gamma-band oscillation effects. Cereb. Cortex 2007, 17:1741-1749.
92. Zion-Golumbic E., Golan T., Anaki D., Bentin S. Human face preference in gamma-frequency EEG activity. Neuroimage 2008, 39:1980-1987.