Direction-selective patterns of activity in human visual cortex suggest common neural substrates for different types of motion

Neuropsychologia

Volumn 50, Issue 4, 2012, Pages 514-521

  Hong, Sang Wook ^a,b   Tong, Frank ^a   Seiffert, Adriane E ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Decoding; Direction selectivity; FMRI; Multivoxel pattern analysis; Second order motion

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVOKED VISUAL RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LUMINANCE; MOTION; NEUROIMAGING; NORMAL HUMAN; RECEPTIVE FIELD; SECONDARY VISUAL CORTEX; SPATIAL DISCRIMINATION; STRIATE CORTEX; VISUAL AREA V3; VISUAL AREA V4; VISUAL CORTEX; VISUAL FEEDBACK; VISUAL FIELD; VISUAL ORIENTATION; VISUAL STIMULATION; VISUAL THRESHOLD;

BRAIN MAPPING; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MOTION PERCEPTION; NEURONS; PHOTIC STIMULATION; VISUAL CORTEX;

EID: 82955236623     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2011.09.016     Document Type: Article

References (86)

1. Adelson E.H., Bergen J.R. Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 1985, 2:284-299.
2. Al-Haytham, A. I. (1056). Translated in Sabra, A. I. (1989). The Optics of Ibn al-Haytham. Books I-II-III: On direct vision. English Translation and Commentary. 2 Vols., Studies of the Warburg Institute. Vol. 40. London: The Warburg Institute, University of London, ISBN 0-85481-072-2.
3. Allen H.A., Derrington A.M. Slow discrimination of contrast-defined expansion patterns. Vision Research 2000, 40:735-744.
4. Anstis S.M. The perception of apparent movement. Philosophical Transactions of the Royal Society of London, B 1980, 290:153-168.
5. Ashida H., Lingnau A., Wall M.B., Smith A.T. fMRI adaptation reveals separate mechanisms for first-order and second-order motion. Journal of Neurophysiology 2007, 97:1319-1325.
6. Ashida H., Seiffert A.E., Osaka N. Inefficient visual search for second-order motion. Journal of the Optical Society of America A 2001, 18:2255-2266.
7. Baker C.L. Central neural mechanisms for detecting second-order motion. Current Opinion in Neurobiology 1999, 9:461-466.
8. Barraclough N., Tinsley C., Webb B., Vincent C., Derrington A. Processing of first-order motion in marmoset visual cortex is influenced by second-order motion. Visual Neuroscience 2006, 23:815-824.
9. Battelli L., Cavanagh P., Intriligator J., Tramo M.J., Henaff M.A., Michel F., et al. Unilateral right parietal damage leads to bilateral deficit for high-level motion. Neuron 2001, 32:985-995.
10. Benton C.P., Johnston A. A new approach to analyzing texture-defined motion. Proceedings of the Royal Society of London B: Biological Sciences 2001, 268:2435-2443.
11. Benton C.P., Johnston A., McOwan P.W., Victor J.D. Computational modeling of non-Fourier motion: Further evidence for a single luminance-based mechanism. Journal of the Optical Society of America A 2001, 18:2204-2208.
12. Brouwer G.J., van Ee Visual cortex allows prediction of perceptual states during ambiguous structure-from-motion. Journal of Neuroscience 2007, 27:1015-1023.
13. Cavanagh P. Attention-based motion perception. Science 1992, 257:1563-1565.
14. Cavanagh P., Mather G. Motion: The long and short of it. Spatial Vision 1989, 4:103-129.
15. Chaudhuri A., Albright T.D. Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1. Visual Neuroscience 1997, 14:949-962.
16. Chubb C., Sperling G. Drift-balanced random stimuli: A general basis for studying non-Fourier motion perception. Journal of the Optical Society of America A 1988, 5:1986-2007.
17. Claeys K.G., Lindsey D.T., De Schutter E., Orban G.A. A higher order motion region in human inferior parietal lobule: Evidence from fMRI. Neuron 2003, 40:631-642.
18. Cowey A., Campana G., Walsh V., Vaina L.M. The role of human extra-striate visual areas V5/MT and V2/V3 in the perception of the direction of global motion: A transcranial magnetic stimulation study. Experimental Brain Research 2006, 171:558-562.
19. Del Viva M.M., Morrone C.M. Motion analysis by feature tracking. Vision Research 1998, 38:3633-3653.
20. Derrington A.M., Allen H.A., Delicato L.S. Visual mechanisms of motion analysis and motion perception. Annual Review of Psychology 2004, 55:181-205.
21. Derrington A.M., Badcock D.R. Separate detectors for simple and complex gratings pattern?. Vision Research 1985, 25:1869-1878.
22. DeYoe E.A., Carman G.J., Bandettini P., Glickman S., Wieser J., Cox R., et al. Mapping striate and extrastriate visual areas in human cerebral cortex. Proceedings of the National Academy of Sciences United States of America 1996, 93:2382-2386.
23. Dumoulin S.O., Baker C.L., Hess R.F., Evans A.C. Cortical specialization for processing first- and second-order motion. Cerebral Cortex 2003, 13:1375-1385.
24. Engel S.A., Glover G.H., Wandell B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cerebral Cortex 1997, 7:181-192.
25. Federspiel A., Volpe U., Horn H., Dierks T., Franck A., Vannini P., et al. Motion standstill leads to activation of inferior parietal lobe. Human Brain Mapping 2006, 27(4):340-349.
26. Formisano E., De Martino F., Bonte M., Goebel R. Who is saying What? Brain-based decoding of human voice and speech. Science 2008, 322:970-973.
27. Greenlee M.W., Smith A.T. Detection and discrimination of first- and second-order motion in patients with unilateral brain damage. Journal of Neuroscience 1997, 17:804-818.
28. Grossman E.D., Blake R. Brain activity evoked by inverted and imagined biological motion. Vision Research 2001, 41:1475-1482.
29. Grossman E.D., Blake R. Brain areas active during visual perception of biological motion. Neuron 2002, 35:1167-1175.
30. Harrison S.A., Tong F. Decoding reveals the contents of visual working memory in early visual areas. Nature 2009, 458:632-635.
31. Ho C.E. Letter recognition reveals pathways of second-order and third-order motion. Proceedings of the National Academy of Sciences United States of America 1998, 95:400-404.
32. Hutchinson C.V., Ledgeway T. Sensitivity to spatial and temporal modulations of first-order and second-order motion. Vision Research 2006, 46:324-335.
33. Hutchinson C.V., Ledgeway T. Temporal frequency modulates reaction time responses to first-order and second-order motion. Journal of Experimental Psychology: Human Perception and Performance 2010, 36:1325-1332.
34. Johnston A., Clifford C.W.G. A unified account of three apparent motion illusions. Vision Research 1995, 35:1109-1123.
35. Johnston A., McOwen P.W., Buxton H. A computation model of the analysis of some first-order and second-order motion patterns by simple and complex cells. Proceedings of the Royal Society of London B: Biological Sciences 1992, 250:297-306.
36. Kamitani Y., Tong F. Decoding the visual and subjective contents of the human brain. Nature Neuroscience 2005, 8:679-685.
37. Kamitani Y., Tong F. Decoding seen and attended motion directions from activity in the human visual cortex. Current Biology 2006, 16:1096-1102.
38. Kriegeskorte N., Mur M., Ruff D.A., Kiani R., Bodurka J., Esteky H., et al. Matching categorical object representations in inferior temporal cortex of man and monkey. Neuron 2008, 60:1126-1141.
39. Ledgeway T. Adaptation to second-order motion results in a motion aftereffect for directionally-ambiguous test stimuli. Vision Research 1994, 34:2879-2889.
40. Ledgeway T., Hutchinson C.V. The influence of spatial and temporal noise on the detection of first-order and second-order orientation and motion direction. Vision Research 2005, 45:2081-2094.
41. Ledgeway T., Smith A.T. Evidence for separate motion detecting mechanisms for first- and second-order motion in human vision. Vision Research 1994, 34:2727-2740.
42. Ledgeway T., Smith A.T. Changes in perceived speed following adaptation to first-order and second-order motion. Vision Research 1997, 37:215-224.
43. Ledgeway T., Zhan C., Johnson A.P., Song Y., Baker C.L. The direction-selective contrast response of area 18 neurons is different for first- and second-order motion. Visual Neuroscience 2005, 22:87-99.
44. Lu Z-L., Sperling G. The functional architecture of human visual motion perception. Vision Research 1995, 35:2697-2772.
45. McCarthy J.E. Directional adaptation effects with contrast modulated stimuli. Vision Research 1993, 33:2653-2662.
46. Mitchell T.M., Shinkareva S.V., Carlson A., Chang K.M., Malave V.L., Mason R.A., et al. Predicting human brain activity associated with the meanings of nouns. Science 2008, 320:1191-1195.
47. Naselaris T., Prenger R.J., Kay K.N., Oliver M., Gallant J.L. Bayesian reconstruction of natural images from human brain activity. Neuron 2009, 63:902-915.
48. Nishida S., Ledgeway T., Edwards M. Dual multiple-scale processing for motion in the human visual system. Vision Research 1997, 37:2685-2698.
49. Nishida S., Sasaki Y., Murakami I., Watanabe T., Tootell R.B. Neuroimaging of direction-selective mechanisms for second-order motion. Journal of Neurophysiology 2003, 90:3242-3254.
50. Noguchi Y., Kaneoke Y., Kakigi R., Tanabe H.C., Sadato N. Role of superior temporal region in human visual motion perception. Cerebral Cortex 2005, 15:1592-1601.
51. O'Keefe L.P., Movshon J.A. Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey. Visual Neuroscience 1998, 15:305-317.
52. Pavan A., Campana G., Guerreschi M., Manassi M., Casco C. Separate motion-detecting mechanisms for first- and second-order patterns revealed by rapid forms of visual motion priming and motion aftereffect. Journal of Vision 2009, 9(11):27. 1-16, http://journalofvision.org/9/11/27/. 10.1167/9.11.27.
53. Plant G.T., Laxer K.D., Barbaro N.M., Schiffman J.S., Nakayama K. Impaired visual motion perception in the contralateral hemifield following unilateral posterior cerebral lesions. Brain 1993, 116:1303-1335.
54. Plant G.T., Nakayama K. The characteristics of residual motion perception in the hemifield contralateral to lateral occipital lesions in humans. Brain 1993, 116:1337-1353.
55. Poldrack R.A., Halchenko Y.O., Hanson S.J. Decoding the large-scale structure of brain function by classifying mental States across individuals. Psychological Science 2009, 20:1364-1372.
56. Rizzo M., Nawrot M., Sparks J., Dawson J. First and second-order motion perception after focal human brain lesions. Vision Research 2008, 48:2682-2688.
57. Ruff C.C., Bestmann S., Blankenburg F., Bjoertomt O., Josephs O., Weiskopf N., et al. Distinct causal influences of parietal versus frontal areas on human visual cortex: Evidence from concurrent TMS-fMRI. Cerebral Cortex 2008, 18(4):817-827.
58. Sawamura H., Orban G.A., Vogels R. Selectivity of neuronal adaptation does not match response selectivity: A single-cell study of the fMRI adaptation paradigm. Neuron 2006, 49:307-318.
59. Seiffert A.E., Cavanagh P. Position displacement, not velocity, is the cue to motion detection of second-order stimuli. Vision Research 1998, 38:3569-3582.
60. Seiffert A.E., Cavanagh P. Position-based motion perception for color and texture stimuli: Effects of contrast and speed. Vision Research 1999, 39:4172-4185.
61. Seiffert A.E., Somers D.C., Dale A.M., Tootell R.B. Functional MRI studies of human visual motion perception: Texture, luminance, attention and aftereffects. Cerebral Cortex 2003, 13:340-349.
62. Serences J.T., Boynton G.M. Feature-based attentional modulations in the absence of direct visual stimulation. Neuron 2007, 55:301-312.
63. Serences J.T., Boynton G.M. The representation of behavioral choice for motion in human visual cortex. Journal of Neuroscience 2007, 27:12893-12899.
64. Serences J.T., Ester E.F., Vogel E.K., Awh E. Stimulus-specific delay activity in human primary visual cortex. Psychological Science 2009, 20:207-214.
65. Sereno M.I., Dale A.M., Reppas J.B., Kwong K.K., Belliveau J.W., Brady T.J., et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 1995, 268:889-893.
66. Seymour K.J., Clifford C.W.G., Logothetis N.K., Bartels A. The coding of color, motion and their conjunction in the human visual cortex. Current Biology 2009, 19:177-183.
67. Smith A.T., Greenlee M.W., Singh K.D., Kraemer F.M., Henning J. The processing of first- and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). Journal of Neuroscience 1998, 18:3816-3830.
68. Swisher J.D., Gatenby J.C., Gore J.C., Wolfe B.A., Moon C.-H., Kim S.-G., et al. Multiscale pattern analysis of orientation-selective activity in the primary visual cortex. Journal of Neuroscience 2010, 30:325-330.
69. Tolias A.S., Keliris G.A., Smirnakis S.M., Logothetis N.K. Neurons in macaque area V4 acquire directional tuning after adaptation to motion stimuli. Nature Neuroscience 2005, 8:591-593.
70. Tong, F., & Pratte, M. S. (2012). Decoding patterns of human brain activity. Annual Review in Psychology. doi:10.1146/annurev-psych-120710-100412.
71. Ukkonen O.I., Derrington A.M. Motion of contrast-modulated gratings is analysed by different mechanisms at low and at high contrasts. Vision Research 2000, 40:3359-3371.
72. Ullman S. The interpretation of visual motion 1979, MIT Press, Cambridge, MA.
73. Vaina L.M., Cowey A. Impairment of the perception of second order motion but not first order motion in a patient with unilateral focal brain damage. Proceedings of the Royal Society of London B: Biological Sciences 1996, 263:1225-1232.
74. Vaina L.M., Cowey A., Kennedy D. Perception of first- and second-order motion: Separable neurological mechanisms?. Human Brain Mapping 1999, 7:67-77.
75. Vaina L.M., Dumoulin S.O. Neuropsychological evidence for three distinct motion mechanisms. Neuroscience Letters 2011, 495:102-106.
76. Vaina L.M., Makris N., Kennedy D., Cowey A. The neuroanatomical damage producing selective deficits to first or second order motion in stroke patients provides further evidence for separate mechanisms. NeuroImage 1996, 3:S360.
77. Vaina L.M., Makris N., Kennedy D., Cowey A. The selective impairment of the perception of first-order motion by unilateral cortical brain damage. Visual Neuroscience 1998, 15:333-348.
78. Vaina L.M., Soloviev S. First-order and second-order motion: Neurological evidence for neuroanatomically distinct system. Progress in Brain Research 2004, 144:197-212.
79. Vaina L.M., Soloviev S., Bienfang D.C., Cowey A. A lesion of cortical area V2 selectively impairs the perception of the direction of first-order visual motion. Neuroreport 2000, 11:1039-1044.
80. van Santen J.P.H., Sperling G. Elaborated Reichardt detectors. Journal of the Optical Society of America A 1985, 2:300-321.
81. Watson A.B., Ahumada A.J. Model of human visual-motion sensing. Journal of the Optical Society of America A 1985, 2:322-341.
82. Wertheimer M. Experimentelle Studien uber das Sehen von Bewegung. Zeitschrift fur Psychologie 1912, 61:161-265. Partial English translation in Thorne Shipley (Ed.). (1961). Classics in psychology. New York: Philosophical Library, pp. 1032-1089.
83. Whitney D., Goltz H.C., Thomas C.G., Gati J.S., Menon R.S., Goodale M.A. Flexible retinotopy: Motion-dependent position coding in the visual cortex. Science 2003, 302:878-881.
84. Wilson H.R., Ferrera V.P., Yo C. A psychophysically motivated model for two-dimensional motion perception. Visual Neuroscience 1992, 9:79-97.
85. Zhou Y., Baker C.L. A processing stream in mammalian visual cortex neurons for non-Fourier responses. Science 1993, 261:98-101.
86. Zhou Y., Baker C.L. Envelope-responsive neurons in areas 17 and 18 of cat. Journal of Neurophysiology 1994, 72:2134-2150.