Retinotopic and lateralized processing of spatial frequencies in human visual cortex during scene categorization

Journal of Cognitive Neuroscience

Volumn 25, Issue 8, 2013, Pages 1315-1331

  Musel, Benoit ^a,b   Bordier, Cécile ^b,c   Dojat, Michel ^b,c   Pichat, Cédric ^a,b   Chokron, Sylvie ^d,e   Le Bas, Jean François ^f   Peyrin, Carole ^a,b  

^a UNIVERSITÉ PIERRE MENDÈS FRANCE   (France)

^b UNIV GRENOBLE ALPES   (France)

^c GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^d FONDATION OPHTALMOLOGIQUE ADOLPHE DE ROTHSCHILD   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CALCARINE SULCUS; CLINICAL ARTICLE; CUNEUS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; LINGUAL GYRUS; MALE; MIDDLE TEMPORAL GYRUS; OCCIPITAL CORTEX; OCCIPITAL GYRUS; OCCIPITAL LOBE; PARAHIPPOCAMPAL GYRUS; PHOTOGRAPHY; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SUPERIOR FRONTAL GYRUS; TEMPORAL CORTEX; VISUAL CORTEX; VISUAL FIELD; VISUAL MEMORY; BRAIN MAPPING; DEPTH PERCEPTION; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PHOTOSTIMULATION; PHYSIOLOGY; REACTION TIME; RECOGNITION; VASCULARIZATION; VISUAL SYSTEM; YOUNG ADULT;

OXYGEN;

ADULT; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REACTION TIME; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS; YOUNG ADULT;

EID: 84879945181     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn_a_00397     Document Type: Article

References (91)

1. Baciu, M., Juphard, A., Cousin, E., & Le Bas, J. F. (2005). Evaluating fMRI methods for assessing hemispheric language dominance in healthy subjects. European Journal of Radiology, 55, 209-218.
2. Badcock, J. C., Whitworth, F. A., Badcock, D. R., & Lovegrove, W. J. (1990). Low-frequency filtering and the processing of local-global stimuli. Perception, 19, 617-629.
3. Bar, M. (2003). A cortical mechanism for triggering top-down facilitation in visual object recognition. Journal of Cognitive Neuroscience, 15, 600-609.
4. Bartels, A., & Zeki, S. (2000). The architecture of the colour centre in the human visual brain: New results and a review. European Journal of Neuroscience, 12, 172-193.
5. Brefczynski, J. A., & DeYoe, E. A. (1999). A physiological correlate of the "spotlight" of visual attention. Nature Neuroscience, 2, 370-374.
6. Brewer, A. A., Liu, J., Wade, A. R., & Wandell, B. A. (2005). Visual field maps and stimulus selectivity in human ventral occipital cortex. Nature Neuroscience, 8, 1102-1109.
7. Buchsbaum, M. S., Buchsbaum, B. R., Chokron, S., Tang, C., Wei, T. C., & Byne, W. (2006). Thalamocortical circuits: Fmri assessment of the pulvinar and medial dorsal nucleus in normal volunteers. Neuroscience Letters, 404, 282-287.
8. Bullier, J. (2001). Integrated model of visual processing. Brain Research Reviews, 36, 96-107.
9. Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12, 1-47.
10. Chokron, S., Brickman, A. M., Wei, T., & Buchsbaum, M. S. (2000). Hemispheric asymmetry for selective attention. Cognitive Brain Research, 9, 85-90.
11. Christman, S., Kitterle, F. L., & Hellige, J. (1991). Hemispheric asymmetry in the processing of absolute versus relative spatial frequency. Brain and Cognition, 16, 62-73.
12. Cousin, E., Peyrin, C., & Baciu, M. (2006). Hemispheric predominance assessment of phonology and semantics: A divided visual Weld experiment. Brain and Cognition, 61, 298-304.
13. Curcio, C. A., & Allen, K. A. (1990). Topography of ganglion cells in human retina. The Journal of Comparative Neurology, 300, 5-25.
14. Curcio, C. A., Sloan, K. R., Kalina, R. E., & Hendrickson, A. E. (1990). Human photoreceptor topography. The Journal of Comparative Neurology, 292, 497-523.
15. Cusack, R., & Papadakis, N. (2002). New robust 3-D phase unwrapping algorithms: Application to magnetic field mapping and undistorting echoplanar images. Neuroimage, 16, 754-764.
16. De Valois, R. L., Albrecht, D. G., & Thorell, L. G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research, 22, 545-559.
17. De Valois, R. L., Yund, E. W., & Hepler, N. (1982). The orientation and direction selectivity of cells in macaque visual cortex. Vision Research, 22, 531-544.
18. Deichmann, R., Good, C. D., Josephs, O., Ashburner, J., & Turner, R. (2000). Optimization of 3-D MP-RAGE sequences for structural brain imaging. Neuroimage, 12, 112-127.
19. Dougherty, R. F., Koch, V. M., Brewer, A. A., Fischer, B., Modersitzki, J., & Wandell, B. A. (2003). Visual field representations and locations of visual areas V1/2/3 in human visual cortex. Journal of Vision, 3, 586-598.
20. Downing, P. E., Chan, A. W. Y., Peelen, M. V., Dodds, C. M., & Kanwisher, N. (2006). Domain specificity in visual cortex. Cerebral Cortex, 16, 1453-1461.
21. Engel, S. A., Glover, G. H., & Wandell, B. A. (1997). Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cerebral Cortex, 7, 181-192.
22. Epstein, R. A. (2008). Parahippocampal and retrosplenial contributions to human spatial navigation. Trends in Cognitive Sciences, 12, 388-396.
23. Epstein, R. A., Harris, A., Stanley, D., & Kanwisher, N. (1999). The parahippocampal place area: Recognition, navigation, or encoding? Neuron, 23, 115-125.
24. Epstein, R. A., & Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature, 392, 598-601.
25. Everson, R. M., Prashanth, A. K., Gabbay, M., Knight, B. W., Sirovich, L., & Kaplan, E. (1998). Representation of spatial frequency and orientation in the visual cortex. Proceedings of the National Academy of Sciences, U.S.A., 95, 8334-8338.
26. Field, D. J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A, 4, 2379-2394.
27. Fink, G. R., Halligan, P. W., Marshall, J. C., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1996). Where in the brain does visual attention select the forest and the trees? Nature, 382, 626-628.
28. Foster, K. H., Gaska, J. P., Nagler, M., & Pollen, D. A. (1985). Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. The Journal of Physiology, 365, 331-363.
29. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. B., Frith, C. D., & Frackowiak, R. S. J. (1995). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2, 189-210.
30. Gandhi, S. P., Heeger, D. J., & Boynton, G. M. (1999). Spatial attention affects brain activity in human primary visual cortex. Proceedings of the National Academy of Sciences, U.S.A., 96, 3314-3319.
31. Gegenfurtner, K. R., Kiper, D. C., & Levitt, J. B. (1997). Functional properties of neurons in macaque area V3. Journal of Neurophysiology, 77, 1906-1923.
32. Ginsburg, A. P. (1986). Spatial filtering and visual form perception. In K. Boff, L. Kauman, & J. Thomas (Eds.), Handbook of perception and human performance (Vol. II, chap. 34, pp. 1-41). New York: Wiley.
33. Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20-25.
34. Grabowska, A., & Nowicka, A. (1996). Visual-spatial-frequency model of cerebral asymmetry: A critical survey of behavioral and electrophysiological studies. Psychological Bulletin, 120, 434-449.
35. Guyader, N., Chauvin, A., Peyrin, C., Herault, J., & Marendaz, C. (2004). Image phase or amplitude? Rapid scene categorization is an amplitude-based process. Comptes Rendus Biologies, 327, 313-318.
36. Han, S., Weaver, J. A., Murray, S. O., Kang, X., Yund, E. W., & Woods, D. L. (2002). Hemispheric asymmetry in global/ local processing: Effects of stimulus position and spatial frequency. Neuroimage, 17, 1290-1299.
37. Hegdé, J. (2008). Time course of visual perception: Coarse-to-fine processing and beyond. Progress in Neurobiology, 84, 405-439.
38. Heinze, H. J., Hinrichs, H., Scholz, M., Burchert, W., & Mangun, G. R. (1998). Neural mechanisms of global and local processing: A combined PET and ERP study. Journal of Cognitive Neuroscience, 10, 485-498.
39. Henriksson, L., Nurminen, L., Hyvärinen, A., & Vanni, S. (2008). Spatial frequency tuning in human retinotopic visual areas. Journal of Vision, 8, 1-13.
40. Holmes, G. (1918). Disturbances of vision by cerebral lesions. British Journal of Ophthalmology, 2, 353-384.
41. Horton, J. C., & Hoyt, W. F. (1991). The representation of the visual field in human striate cortex: A revision of the classic Holmes map. Archives of Ophthalmology, 109, 816.
42. Hughes, H. C., Nozawa, G., & Kitterle, F. L. (1996). Global precedence, spatial frequency channels, and the statistic of the natural image. Journal of Cognitive Neuroscience, 8, 197-230.
43. Hutton, C., Bork, A., Josephs, O., Deichmann, R., Ashburner, J., & Turner, R. (2002). Image distortion correction in fMRI: A quantitative evaluation. Neuroimage, 16, 217-240.
44. Iidaka, T., Yamashita, K., Kashikura, K., & Yonekura, Y. (2004). Spatial frequency of visual image modulates neural responses in the temporo-occipital lobe. An investigation with eventrelated fMRI. Cognitive Brain Research, 18, 196-204.
45. Issa, N. P., Trepel, C., & Stryker, M. P. (2000). Spatial frequency maps in cat visual cortex. The Journal of Neuroscience, 20, 8504-8514.
46. Kaas, J. H. (1997). Theories of visual cortex organization in primates. In J. H. Kaas, K. S. Rockland, & A. Peters (Eds.), Cerebral cortex (pp. 91-125). New York: Plenum.
47. Kenemans, J. L., Baas, J. M. P., Mangun, G. R., Lijffijt, M., & Verbaten, M. N. (2000). On the processing of spatial frequencies as revealed by evoked-potential source modeling. Clinical Neurophysiology, 111, 1113-1123.
48. Kitterle, F. L., Christman, S., & Hellige, J. B. (1990). Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies. Attention, Perception, & Psychophysics, 48, 297-306.
49. Lamb, M. R., Robertson, L. C., & Knight, R. T. (1990). Component mechanisms underlying the processing of hierarchically organized patterns: Inferences from patients with unilateral cortical lesions. Journal of Experimental Psychology: Learning, Memory, and Cognition, 16, 471-483.
50. Lamb, M. R., & Yund, E. W. (1993). The role of spatial frequency in the processing of hierarchically organized stimuli. Attention, Perception, & Psychophysics, 54, 773-784.
51. Lorenson, W., & Cline, H. (1987). Marching cubes, a high resolution 3D surface construction algorithm. Computer Graphics, 21, 163-169.
52. Lux, S., Marshall, J. C., Ritzl, A., Weiss, P. H., Pietrzyk, U., Shah, N. J., et al. (2004). A functional magnetic resonance imaging study of local/global processing with stimulus presentation in the peripheral visual hemifields. Neuroscience, 124, 113-120.
53. Martinez, A., Anllo-Vento, L., Sereno, M. I., Frank, L. R., Buxton, R. B., Dubowitz, D. J., et al. (1999). Involvement of striate and extrastriate visual cortical areas in spatial attention. Nature Neuroscience, 2, 364-369.
54. Martinez, A., Di Russo, F., Anllo-Vento, L., & Hillyard, S. A. (2001). Electrophysiological analysis of cortical mechanisms of selective attention to high and low spatial frequencies. Clinical Neurophysiology, 112, 1980-1998.
55. Martinez, A., Moses, P., Frank, L., Buxton, R., Wong, E., & Stiles, J. (1997). Hemispheric asymmetries in global and local processing: Evidence from fMRI. NeuroReport, 8, 1685-1689.
56. Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neurosciences, 6, 414-417.
57. Musel, B., Hera, R., Chokron, S., Alleysson, D., Chiquet, C., Romanet, J. P., et al. (2011). Residual abilities in age-related macular degeneration patients to process spatial frequencies during natural scenes categorization. Visual Neuroscience, 28, 529-541.
58. Navon, D. (1977). Forest before trees: The precedence of global features in visual perception. Cognitive Psychology, 9, 353-383.
59. Peyrin, C., Baciu, M., Segebarth, C., & Marendaz, C. (2004). Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition, an event-related fMRI study. Neuroimage, 23, 698-707.
60. Peyrin, C., Chauvin, A., Chokron, S., & Marendaz, C. (2003). Hemispheric specialization for spatial frequency processing in the analysis of natural scenes. Brain and Cognition, 53, 278-282.
61. Peyrin, C., Chokron, S., Guyader, N., Gout, O., Moret, J., & Marendaz, C. (2006). Neural correlates of spatial frequency processing: A neuropsychological approach. Brain Research, 74, 1-10.
62. Peyrin, C., Mermillod, M., Chokron, S., & Marendaz, C. (2006). Effect of temporal constraints on hemispheric asymmetries during spatial frequency processing. Brain and Cognition, 62, 214-220.
63. Peyrin, C., Michel, C. M., Schwartz, S., Thut, G., Seghier, M., Landis, T., et al. (2010). The neural substrates and timing of top-down processes during coarse-to-fine categorization of visual scenes: A combined fMRI and ERP study. Journal of Cognitive Neuroscience, 22, 2768-2780.
64. Peyrin, C., Schwartz, S., Seghier, M., Michel, C., Landis, T., & Vuilleumier, P. (2005). Hemispheric specialization of human inferior temporal cortex during coarse-to-fine and fine-to-coarse analysis of natural visual scenes. Neuroimage, 28, 464-473.
65. Poggio, G. F. (1972). Spatial properties of neurons in striate cortex of unanesthetized macaque monkey. Investigative Ophthalmology & Visual Science, 11, 368-377.
66. Robertson, L. C., & Lamb, M. R. (1991). Neuropsychological contributions to theories of part/whole organization. Cognitive Psychology, 23, 299-330.
67. Robertson, L. C., Lamb, M. R., & Knight, R. T. (1988). Effects of lesions of temporal-parietal junction on perceptual and attentional processing in humans. The Journal of Neuroscience, 8, 3757-3769.
68. Sasaki, Y., Hadjikhani, N., Fischl, B., Liu, A. K., Marret, S., Dale, A. M., et al. (2001). Local and global attention are mapped retinotopically in human occipital cortex. Proceedings of the National Academy of Sciences, U.S.A., 98, 2077-2082.
69. Scherrer, B., Forbes, F., Garbay, C., & Dojat, M. (2009). Distributed local MRF models for tissue and structure brain segmentation. IEEE Transactions on Medical Imaging, 28, 1278-1295.
70. Schyns, P. G., & Oliva, A. (1994). From blobs to boundary edges: Evidence for time-and spatial-scale-dependant scene recognition. Psychological Science, 5, 195-200.
71. Sereno, M. I., McDonald, C. T., & Allman, J. M. (1994). Analysis of retinotopic maps in extrastriate cortex. Cerebral Cortex, 4, 601-620.
72. Sergent, J. (1982). The cerebral balance of power: Confrontation or cooperation? Journal of Experimental Psychology: Human Perception and Performance, 8, 253-272.
73. Shams, L., & von der Malsburg, C. (2002). The role of complex cells in object recognition. Vision Research, 42, 2547-2554.
74. Shulman, G. L., Sullivan, M. A., Gish, K., & Sakoda, W. J. (1986). The role of spatial-frequency channels in the perception of local and global structure. Perception, 15, 259-273.
75. Singh, K. D., Smith, A. T., & Greenlee, M. W. (2000). Spatio-temporal frequency and direction sensitivities of human visual areas measured using fMRI. Neuroimage, 12, 550-564.
76. Slotnick, S. D., & Moo, L. R. (2006). Prefrontal cortex hemispheric specialization for categorical and coordinate visual spatial memory. Neuropsychologia, 44, 1560-1568.
77. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-Dimensional proportional system: An approach to cerebral imaging. New York: Thieme.
78. Tanaka, K. (1993). Neuronal mechanisms of object recognition. Science, 262, 685.
79. Tolhurst, D. J., Tadmor, Y., & Chao, T. (1992). Amplitude spectra of natural images. Ophthalmic and Physiological Optics, 12, 229-232.
80. Tootell, R. B. H., Hadjikhani, N., Hall, E. K., Marrett, S., Vanduffel, W., Vaughan, J. T., et al. (1998). The retinotopy of visual spatial attention. Neuron, 21, 1409-1422.
81. Tootell, R. B. H., Silverman, M. S., Hamilton, S. L., Switkes, E., & De Valois, R. L. (1988). Functional anatomy of macaque striate cortex. V. Spatial frequency. The Journal of Neuroscience, 8, 1610-1624.
82. Torralba, A., & Oliva, A. (2003). Statistics of natural image categories. Network: Computation in Neural Systems, 14, 391-412.
83. Tulving, E., Markowitsch, H. J., Kapur, S., & Habib, R. (1994). Novelty encoding networks in the human brain: Positron emission tomography data. NeuroReport, 5, 2525-2528.
84. Vasseur, F., Delon-Martin, C., Warnking, J., Segebarth, C., & Dojat, M. (2010). fMRI retinotopic mapping at 3T: Benefits gained from correcting the spatial distortions due to static field inhomogeneity. Journal of Vision, 10, 1-12.
85. Wade, A. R., Brewer, A. A., Rieger, J. W., & Wandell, B. A. (2002). Functional measurements of human ventral occipital cortex: Retinotopy and color. Philosophical Transactions of the Royal Society of London, Series B, Biologicial Sciences, 357, 963-973.
86. Wandell, B. A., Brewer, A. A., & Dougherty, R. F. (2005). Visual field map clusters in human cortex. Philosophical Transactions of the Royal Society of London, Series B, Biologicial Sciences, 360, 693-707.
87. Warnking, J., Dojat, M., Guérin-Dugué, A., Delon-Martin, C., Olympieff, S., Richard, N., et al. (2002). fMRI retinotopic mapping-Step by step. Neuroimage, 17, 1665-1683.
88. Watanabe, T., Sasaki, Y., Miyauchi, S., Putz, B., Fujimaki, N., Nielsen, M., et al. (1998). Attention-regulated activity in human primary visual cortex. Journal of Neurophysiology, 79, 2218-2221.
89. Xu, X., Anderson, T. J., & Casagrande, V. A. (2007). How do functional maps in primary visual cortex vary with eccentricity? The Journal of Comparative Neurology, 501, 741-755.
90. Yamaguchi, S., Yamagata, S., & Kobayashi, S. (2000). Cerebral asymmetry of the "top-down" allocation of attention to global and local features. The Journal of Neuroscience, 20, RC72.
91. Zeki, S., Watson, J. D., Lueck, C. J., Friston, K. J., Kennard, C., & Frackowiak, R. S. (1991). A direct demonstration of functional specialization in human visual cortex. The Journal of Neuroscience, 11, 641-649.