Event-related functional MRI of cortical activity evoked by microsaccades, small visually-guided saccades, and eyeblinks in human visual cortex

NeuroImage

Volumn 49, Issue 1, 2010, Pages 805-816

  Tse, Peter U ^a   Baumgartner, Florian J ^b   Greenlee, Mark W ^b  

^a Dartmouth College   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; EVENT RELATED POTENTIAL; EXCITATION; EYE MOVEMENT; EYELID REFLEX; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; RECORDING; RETINA GANGLION CELL; SACCADIC EYE MOVEMENT; STIMULUS RESPONSE; VISUAL CORTEX; VISUAL SYSTEM;

ADULT; BLINKING; BRAIN MAPPING; EVOKED POTENTIALS; FEMALE; FIXATION, OCULAR; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OPTICAL ILLUSIONS; OXYGEN; PHOTIC STIMULATION; SACCADES; VISUAL CORTEX;

EID: 70350015371     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.07.052     Document Type: Article

References (105)

1. Bair W., and O'Keefe L.P. The influence of fixational eye movements on the response of neurons in area hMT+ of the macaque. Vis. Neurosci. 15 (1998) 779-786
2. Barlow H.B. Eye movements during fixation. J.Physiol. Lond. 116 (1952) 290-306
3. Beeler G.W. Visual threshold changes resulting from spontaneous saccadic eye movements. Vis. Res. 7 (1967) 769-775
4. Bender D.B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res. 279 (1983) 258-261
5. Bridgeman B.B., and Macknik S.L. Saccadic suppression relies on luminance information. Psychol. Res. 58 (1995) 163-168
6. Bridgeman B., and Palca J. The role of microsaccades in high acuity observational tasks. Vision Res. 20 (1980) 813-817
7. Burr D.C., Morrone M.C., and Ross J. Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371 6497 (1994) 511-513
8. Clarke F.J., and Belcher S.J. On the localization of Troxler's effect in the visual pathway. Vis. Res. 2 (1962) 53-68
9. Corbetta M., Akbudak E., Conturo T.E., Snyder A.Z., Ollinger J.M., Drury H.A., Linenweber M.R., Petersen S.E., Raichle M.E., Van Essen D.C., and Shulman G.L. A common network of functional areas for attention and eye movements. Neuron 21 4 (1998) 761-773
10. Cynader M., and Berman N. Receptive-field organization of monkey superior colliculus. J. Neurophysiol. 35 (1972) 187-201
11. Ditchburn R.W. Eye-movements in relation to retinal action. Opt. Acta Lond. 1 (1955) 171-176
12. Ditchburn R.W., and Ginsborg B.L. Involuntary eye movements during fixation. J. Physiol. 119 (1953) 1-17
13. Engbert R. Microsaccades: a microcosm for research on oculomotor control attention and visual perception. Prog. Brain Res. 154 (2006) 177-192
14. Engbert R., and Kliegl R. Microsaccades uncover the orientation of covert attention. Vis. Res. 43 (2003) 1035-1045
15. Engbert R., and Kliegl R. Microsaccades keep the eyes' balance during fixation. Psychol. Sci. 6 (2004) 431-436
16. Everling S., and Munoz D.P. Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J. Neurosci. 20 1 (2000) 387-400
17. Fiorentini A., and Ercoles A.M. Involuntary eye movements during attempted monocular fixation. Atti Fond. Giorgio Ronchi 21 (1966) 199-217
18. Fox P.T., and Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. 83 (1986) 1140-1144
19. Frahm J., Krüger G., Merboldt K.D., and Kleinschmidt A. Dynamic uncoupling and recoupling of perfusion and oxidative metabolism during focal brain activation in man. Magn. Reson. Med. 35 (1996) 143-148
20. Frostig R.D., Lieke E.E., Tso D.Y., and Grinvald A. Cortical functional architecture ad local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc. Natl. Acad. Sci. 87 (1990) 6082-6086
21. Greschner M., Bongard M., Rujan P., and Ammermuller J. Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature 5 (2002) 341-347
22. Gur M., and Snodderly D.M. Visual receptive fields of neurons in primary visual cortex (V1) move in space with the eye movements of fixation. Vis. Res. 37 (1997) 257-265
23. Gur M., Beylin A., and Snodderly D.M. Response variability of neurons in primary visual cortex (V1) of alert monkeys. J. Neurosci. 17 (1997) 2914-2920
24. Hafed Z.M., and Clark J.J. Microsaccades as an overt measure of covert attention shifts. Vis. Res. 42 (2002) 2533-2545
25. Hafed Z.M., Goffart L., and Krauzlis R.J. A neural mechanism for microsaccade generation in the primate superior colliculus. Science 13 323 5916 (2009) 940-943
26. Hanes D.P., Patterson W.F., and Schall J.D. Role of frontal eye fields in countermanding saccades: visual movement, and fixation activity. J. Neurophysiol. 79 2 (1998) 817-834
27. Hartline H.K. The nerve messages in the fibers of the visual pathway. J.O.S.A. 30 (1940) 239-247
28. Horwitz G.D., and Albright T.D. Short-latency fixational saccades induced by luminance increments. J. Neurophysiol. 90 (2003) 1333-1339
29. Horowitz T.S., Fine E.M., Fencsik D.E., Yurgenson S., and Wolfe J.M. Fixational eye movements are not an index of covert attention. Psychol. Sci. 18 (2007) 356-363
30. Horowitz T.S., Fine E.M., Fencsik D.E., Yurgenson S., and Wolfe J.M. Microsaccades and attention: does a weak correlation make an index? Reply to Laubrock Engbert Rolfs and Kliegl. Psychol. Sci. 18 4 (2007) 367-368 2
31. Hsieh P.J., and Tse P.U. Microsaccade rate varies with subjective visibility during motion-induced blindness. PLOS One 4 4 (2009) e5163
32. Hubel D.H., and Wiesel T.N. Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 28 (1965) 229-289
33. Huk A.C., Dougherty R.F., and Heeger D.J. Retinotopy and functional subdivision of human areas hMT+ and MST. J. Neurosci. 22 16 (2002) 7195-7205
34. Irwin D.E., Colcombe A.M., Kramer A.F., and Hahn S. Attentional and oculomotor capture by onset luminance and color singletons. Vis. Res. 40 (2000) 1443-1458
35. Jonides J., and Yantis S. Uniqueness of abrupt visual onset in capturing attention. Percept. Psychophys. 43 (1988) 346-354
36. Kagan I., Gur M., and Snodderly D.M. Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion position and extraretinal influences. J. Vis. 8 14 (2008) 1-25 19
37. Kleiser R., Seitz R.J., and Krekelberg B. Neural correlates of saccadic suppression in humans. Curr. Biol. 14 5 (2004) 386-390
38. Kotulak J.C., and Schor C.N. The accommodative response to subthreshold blur and to perceptual fading during the Troxler phenomenon. Perception 15 (1986) 7-15
39. Kowler E., and Steinman R.M. The role of small saccades in counting. Vis. Res. 17 (1977) 141-146
40. Kowler E., and Steinman R.M. Miniature saccades: eye movements that do not count. Vis. Res. 19 (1979) 105-108
41. Krauskopf J. Lack of inhibition during involuntary saccades. Am. J. Psychol. 79 (1966) 73-81
42. Kuffler S.W. Neurons in the retina: organization inhibition and excitation problems. Cold Spring Harbor Symp. Quant. Biol. 17 (1952) 281-292
43. Kustov A.A., and Robinson D.L. Shared neural control of attentional shifts and eye movements. Nature 384 7 (1996) 74-77
44. Laubrock J., Engbert R., Rolfs M., and Kliegl R. Microsaccades are an index of covert attention: Commentary on Horowitz, Fine, Fencsik, Yurgenson and Wolfe (2007). Psychol. Sci. 18 (2007) 364-366
45. Lee P.H., Sooksawate T., Yanagawa Y., Isa K., Isa T., and Hall W.C. Identity of a pathway for saccadic suppression. Proc. Natl. Acad. Sci. U. S. A. 104 16 (2007) 6824-6827
46. Leopold D.A., and Logothetis N.K. Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp. Brain Res. 123 (1998) 341-345
47. Livingstone M.S., and Hubel D.H. Psychophysical evidence for separate channels for the perception of form color movement and depth. J. Neurosci. 7 (1987) 3416-3418
48. Livingstone M.S., Freeman D.C., and Hubel D.H. Visual responses in V1 of freely viewing monkeys. Cold Spring Harbor Symp. Quant. Biol. LXI (1996) 27-37
49. Lord M.P. Measurement of binocular eye movements of subjects in the sitting position. Brit. J. Ophthal. 35 (1951) 21-30
50. Macknik S.L., and Livingstone M.S. Neuronal correlates of visibility and invisibility in the primate visual system. Nat. Neurosci. 1 (1998) 144-149
51. Macknik S.L., Fisher B.D., and Bridgeman B. Flicker distorts visual space constancy. Vis. Res. 31 (1991) 2057-2064
52. Magistretti P.J., and Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999) 1155-1163
53. Martinez-Conde S., Macknik S.L., and Hubel D.H. Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nat. Neurosci. 3 (2000) 251-258
54. Martinez-Conde S., Macknik S.L., and Hubel D.H. The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13920-13925
55. Martinez-Conde S., Macknik S.L., and Hubel D.H. The role of fixational eye movements in visual perception. Nat. Rev. Neurosci. 5 3 (2004) 229-240
56. Martinez-Conde S., Macknik S.L., Troncoso X.G., and Dyar T.A. Microsaccades counteract visual fading during fixation. Neuron 49 2 (2006) 297-305
57. Mesulam M.M. A cortical network for directed attention and unilateral neglect. Ann. Neurol. 10 (1981) 309-325
58. Millodot M. Extra foveal variations of the phenomenon of Troxler. Psychologie Francaise 12 (1967) 190-196
59. Moller F., Laursen M.L., Tygesen J., and Sjolie A.K. Binocular quantification and characterization of microsaccades. Graefes Arch. Clin. Exp. Ophthalmol. 240 (2002) 765-770
60. Munoz D.P., and Wurtz R.H. Fixation cells in monkey superior colliculus II. Reversible activation and deactivation. J. Neurophysiol. 70 2 (1993) 576-589
61. Murakami I., and Cavanagh P.A. A jitter after-effect reveals motion-based stabilization of vision. Nature 395 (1998) 798-801
62. Murakami I., and Cavanagh P. Visual jitter: evidence for visual-motion-based compensation of retinal slip due to small eye movements. Vis. Res. 41 (2001) 173-186
63. Posner M.I., and Petersen S.E. The attention system of the human brain. Annu. Rev. Neurosci. 13 (1990) 25-42
64. Ramachandran V. Blindspot. Scientific American 266 (1992) 4-49
65. Ratliff F., and Riggs L.A. Involuntary motions of the eye during monocular fixation. J. Exp. Psychol. 40 (1950) 687-701
66. Remington R.W., Johnston J.C., and Yantis S. Involuntary attentional capture by abrupt onsets. Percept. Psychophys. 51 (1992) 279-290
67. Reppas J.B., Usrey W.M., and Reid R.C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35 (2002) 961-974
68. Riggs L.A., Ratliff F., Cornsweet J.C., and Cornsweet T.N. The disappearance of steadily fixated visual test objects. J. Opt. Soc. Am. 43 (1953) 495-501
69. Rizzolatti G. In: Umilta C., and Moscovitch E.M. (Eds). Attention and Performance XV (1994), MIT, Cambridge 231-265
70. Robinson D.L., and Kertzman C. Covert orienting of attention in macaques III. Contributions of the superior colliculus. J. Neurophysiol. 74 2 (1995) 713-721
71. Rolfs M., Engbert R., and Kliegl R. Microsaccade orientation supports attentional enhancement opposite to a peripheral cue: commentary on Tse Sheinberg Logothetis. Psychol. Sci 10 (2004) 705-707
72. Rolfs M., Kliegl R., and Engbert R. Toward a model of microsaccade generation: the case of microsaccadic inhibition. J. Vis. 8 11 (2008) 1-23 5
73. Ross J., Morrone M.C., Goldberg M.E., and Burr D.C. Changes in visual perception at the time of saccades. Trends Neurosci. 24 (2001) 113-121
74. Röther J., Knab R., Hamzei F., Fiehler J., Reichenbach J.R., Büchel C., and Weiller C. Negative dip in BOLD fMRI is caused by blood flow-oxygen consumption uncoupling in humans. NeuroImage 15 1 (2002) 98-102
75. Sasaki Y., Murakami I., Cavanagh P., and Tootell R.H. Human brain activity during illusory visual jitter as revealed by functional magnetic resonance imaging. Neuron 35 (2002) 1147-1156
76. Schall J.D. Neural basis of saccade target selection. Rev. Neurosci. 6 1 (1995) 63-85
77. Sereno M.I., Dale A.M., Reppas J.B., Kwong K.K., Belliveau J.W., Brady T.J., Rosen B.R., and Tootell R.B. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268 (1995) 889-893
78. Sincich L.C., Park K.F., Wohlgemuth M.J., and Horton J.C. Bypassing V1: a direct geniculate input to area MT. Nat. Neurosci. 7 10 (2004) 1123-1128
79. Skavenski A.A., Hansen R.M., Steinman R.M., and Winterson B.J. Quality of retinal image stabilization during small natural and artificial body rotations in man. Vis. Res. 19 (1979) 675-683
80. Slotnick S.D., and Yantis S. Efficient acquisition of human retinotopic maps. Hum. Brain Mapp. 18 1 (2003) 22-29
81. Snodderly D.M., Kagan I., and Gur M. Selective activation of visual cortex neurons by fixational eye movements: implications for neural coding. Vis. Neurosci. 18 (2001) 259-277
82. Sotero R.C., and Trujillo-Barreto N.J. Modelling the role of excitatory and inhibitory neuronal activity in the generation of the BOLD signal. NeuroImage 35 1 (2007) 149-165
83. Sparks D.L. The brainstem control of saccadic eye movements. Nat. Rev. Neurosci. 3 (2002) 952-964
84. Sperling G. In: Kowler E. (Ed). Eye Movements and Their Role in Visual and Cognitive Processes (1990), Elsevier 307-351
85. Steinman R.M., Cunitz R.J., Timberlake G.T., and Herman M. Voluntary control of microsaccades during maintained monocular fixation. Science 155 (1967) 1577-1579
86. Steinman R.M., Haddad G.M., Skavenski A.A., and Wyman D. Miniature eye movement. Science 181 (1973) 810-819
87. Theeuwes J. Stimulus-driven capture and attentional set: selective search for color and visual abrupt onsets. J. Exp. Psychol. Hum. Percept. Perform. 20 4 (1994) 799-806
88. Tse P.U., Sheinberg D.L., and Logothetis N.K. Fixational eye movements are not affected by abrupt onsets that capture attention. Vis. Res. 42 (2002) 1663-1669
89. Tse P.U., Sheinberg D.S., and Logothetis N.K. The distribution of microsaccade directions need not reveal the location of attention. Psychol. Sci. 15 10 (2004) 708-710
90. Tse P.U., Caplovitz G.P., and Hsieh P.J. Corrigendum to 'Microsaccade directions do not predict directionality of illusory brightness changes of overlapping transparent surfaces' [Vision Research 46 (2006) 3823-3830]. Vis. Res. 49 790 (2009) e1-e7
91. Turatto M., Valsecchi M., Tamè L., and Betta E. Microsaccades distinguish between global and local visual processing. NeuroReport 18 10 (2007) 1015-1018
92. Vallines I., and Greenlee M.W. Saccadic suppression of retinotopically localized blood oxygen level-dependent responses in human primary visual area V1. J. Neurosci. 26 22 (2006) 5965-5969
93. Valsecchi M., and Turatto M. Microsaccadic response to visual events that are invisible to the superior colliculus. Behav. Neurosci. 121 4 (2007) 786-793
94. Valsecchi M., and Turatto M. Microsaccadic responses in a bimodal oddball task. Psychol. Res. 73 1 (2009) 23-33
95. Winterson B.J., and Collewijn H. Microsaccades during finely guided visuomotor tasks. Vis. Res. 16 (1976) 1387-1390
96. Wurtz R.H. Visual cortex neurons: response to stimuli during rapid eye movements. Science 162 (1968) 1148-1150
97. Wurtz R.H. Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J. Neurophysiol. 32 (1969) 987-994
98. Wurtz R.H. Vision for the control of movement. The Friedenwald lecture. Investig. Ophthalmol. Vis. Sci. 37 (1996) 2130-2145
99. Yantis S., and Hillstrom A.P. Stimulus-driven attentional capture: evidence from equiluminant visual objects. J. Exp. Psychol. Hum. Percept. Perform. 20 1 (1994) 95-107
100. Yantis S., and Jonides J. Abrupt visual onsets and selective attention: evidence from visual search. J. Exp. Psychol. Hum. Percept. Perform. 10 5 (1984) 601-621
101. Yantis S., and Jonides J. Abrupt visual onsets and selective attention: voluntary versus automatic allocation. J. Exp. Psychol. Hum. Percept. Perform. 16 1 (1990) 121-134
102. Yarbus A.L. Eye Movements and Vision (1967), Plenum Press, New York
103. Zuber B.L., and Stark L. Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science 150 (1965) 1459-1460
104. Zuber B.L., and Stark L. Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. Exp. Neurol. 16 (1966) 65-79
105. Zuber B.L., Crider A., and Stark L. Saccadic suppression associated with microsaccades. QPR. 74 (1964) 244-249