From coarse to fine? spatial and temporal dynamics of cortical face processing

Cerebral Cortex

Volumn 21, Issue 2, 2011, Pages 467-476

  Goffaux, Valerie ^a,b   Peters, Judith ^b,c   Haubrechts, Julie ^d   Schiltz, Christine ^a   Jansma, Bernadette ^b   Goebel, Rainer ^b  

^a UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

coarse to fine; exposure duration; face perception; fMRI; spatial frequency

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; DYNAMICS; FACIAL EXPRESSION; FEMALE; FUSIFORM FACE AREA; HUMAN; MALE; OCCIPITAL CORTEX; PRIORITY JOURNAL; SPATIAL FREQUENCY DISCRIMINATION; VISUAL INFORMATION;

ADULT; ANALYSIS OF VARIANCE; BRAIN MAPPING; CEREBRAL CORTEX; FACE; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; PSYCHOPHYSICS; SPACE PERCEPTION; TIME FACTORS; YOUNG ADULT;

EID: 78651470485     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq112     Document Type: Article

References (83)

1. Allen EA, Freeman RD. 2006. Dynamic spatial processing originates in early visual pathways. J Neurosci. 26:11763-11774.
2. Bar M. 2007. The proactive brain: using analogies and associations to generate predictions. Trends Cogn Sci. 11:280-289.
3. Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM, Dale AM, Hamalainen MS, Marinkovic K, Schacter DL, Rosen BR, et al. 2006. Top-down facilitation of visual recognition. Proc Natl Acad Sci USA. 103:449-454.
4. Barton JJ, Press DZ, Keenan JP, O'Connor M. 2002. Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia. Neurology. 58:71-78.
5. Bermudez MA, Vicente AF, Romero MC, Perez R, Gonzalez F. 2009. Spatial frequency components influence cell activity in the inferotemporal cortex. Vis Neurosci. 26:421-428.
6. Bex PJ, Makous W. 2002. Spatial frequency, phase, and the contrast of natural images. J Opt Soc Am A Opt Image Sci Vis. 19:1096-1106.
7. Biederman I. 1987. Recognition-by-components: a theory of human image understanding. Psychol Rev. 94:115-147.
8. Biederman I, Kalocsai P. 1997. Neurocomputational bases of object and face recognition. Philos Trans R Soc Lond B Biol Sci. 352:1203-1219.
9. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 16:4207-4221.
10. Bredfeldt CE, Ringach DL. 2002. Dynamics of spatial frequency tuning in macaque V1. J Neurosci. 22:1976-1984.
11. Bullier J. 2001. Integrated model of visual processing. Brain Res Rev. 36:96-107.
12. Cheung OS, Richler JJ, Palmeri TJ, Gauthier I. 2008. Revisiting the role of spatial frequencies in the holistic processing of faces. J Exp Psychol Hum Percept Perform. 34:1327-1336.
13. Collin CA, Liu CH, Troje NF, McMullen PA, Chaudhuri A. 2004. Face recognition is affected by similarity in spatial frequency range to a greater degree than within-category object recognition. J Exp Psychol Hum Percept Perform. 30:975-987.
14. Collishaw SM, Hole GJ. 2000. Featural and configurational processes in the recognition of faces of different familiarity. Perception. 29:893-909.
15. Dakin SC, Hess RF, Ledgeway T, Achtman RL. 2002. What causes nonmonotonic tuning of fMRI response to noisy images? Curr Biol. 12:R476-R477.; author reply R478.
16. De Heering A, Turati C, Rossion B, Bulf H, Goffaux V, Simion F. 2008. Newborns' face recognition is based on spatial frequencies below 0.5 cycles per degree. Cognition. 106:444-454.
17. De Valois RL, Albrecht DG, Thorell LG. 1982. Spatial frequency selectivity of cells in macaque visual cortex. Vision Res. 22:545-559.
18. De Valois RL, Morgan HC, Snodderly DM. 1974. Psychophysical studies of monkey vision-III. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Res. 14:75-81.
19. Eger E, Schyns PG, Kleinschmidt A. 2004. Scale invariant adaptation in fusiform face-responsive regions. Neuroimage. 22:232-242.
20. Epstein R, Harris A, Stanley D, Kanwisher N. 1999. The parahippocam-pal place area: recognition, navigation, or encoding? Neuron. 23: 115-125.
21. Field DJ. 1987. Relations between the statistics of natural images and the response properties of cortical cells. J Opt Soc Am A. 4:2379-2394.
22. Fiser J, Subramaniam S, Biederman I. 2001. Size tuning in the absence of spatial frequency tuning in object recognition. Vision Res. 41:1931-1950.
23. Flevaris AV, Robertson LC, Bentin S. 2008. Using spatial frequency scales for processing face features and face configuration: an ERP analysis. Brain Res Rev. 1194:100-109.
24. Frazor RA, Albrecht DG, Geisler WS, Crane AM. 2004. Visual cortex neurons of monkeys and cats: temporal dynamics of the spatial frequency response function. J Neurophysiol. 91:2607-2627.
25. Gauthier I, Curby KM, Skudlarski P, Epstein RA. 2005. Individual differences in FFA activity suggest independent processing at different spatial scales. Cogn Affect Behav Neurosci. 5:222-234.
26. Goffaux V, Gauthier I, Rossion B. 2003. Spatial scale contribution to early visual differences between face and object processing. Brain Res Cogn Brain Res. 16:416-424.
27. Goffaux V, Hault B, Michel C, Vuong QC, Rossion B. 2005. The respective role of low and high spatial frequencies in supporting configural and featural processing of faces. Perception. 34:77-86.
28. Goffaux V, Rossion B. 2006. Faces are "spatial"-holistic face perception is supported by low spatial frequencies. J Exp Psychol Hum Percept Perform. 32:1023-1039.
29. Goffaux V, Rossion B, Sorger B, Schiltz C, Goebel R. 2009. Face inversion disrupts the perception of vertical relations between features in the right human occipito-temporal cortex. J Neuropsychol. 3:45-67.
30. Gold J, Bennett PJ, Sekuler AB. 1999. Identification of band-pass filtered letters and faces by human and ideal observers. Vision Res. 39:3537-3560.
31. Halit H, de Haan M, Schyns PG, Johnson MH. 2006. Is high-spatial frequency information used in the early stages of face detection? Brain Res. 1117:154-161.
32. Hansen BC, Essock EA. 2004. A horizontal bias in human visual processing of orientation and its correspondence to the structural components of natural scenes. J Vis. 10:1044-60.
33. Haxby JV, Hoffman EA, Gobbini MI. 2000. The distributed human neural system for face perception. Trends Cogn Sci. 4:223-233.
34. Hegde J. 2008. Time course of visual perception: coarse-to-fine processing and beyond. Prog Neurobiol. 84:405-439.
35. Hess RF. 2004. Spatial scale in visual processing. In: Chalupa LM, Werner JS, editors. The visual neurosciences. Cambridge (MA): MIT Press. p. 1043-1059.
36. Hochstein S, Ahissar M. 2002. View from the top: hierarchies and reverse hierarchies in the visual system. Neuron. 36:791-804.
37. Hughes HC, Nozawa G, Kitterle F. 1996. Global precedence, spatial frequency channels, and the statistics of natural images. J Cogn Neurosci. 8:197-230.
38. Iidaka T, Yamashita K,Kashikura K, Yonekura Y. 2004. Spatial frequency of visual image modulates neural responsesin the temporo-occipital lobe. An investigation with event-related fMRI. Cogn Brain Res. 18:196-204.
39. Kanwisher N, McDermott J, Chun MM. 1997. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci. 17:4302-4311.
40. Kaplan E. 2004. The M, P and K pathways of the primate visual system. In: Chalupa LM, Werner JS, editors. The visual neurosciences. Cambridge (MA): MIT Press. p. 1043-1059.
41. Keysers C, Perrett DI. 2002. Visual masking and RSVP reveal neural competition. Trends Cogn Sci. 6:120-125.
42. Konar Y, Bennett PJ, Sekuler AB. 2010. Holistic processing is not correlated with face-identification accuracy. Psychol Sci. 21:38-43.
43. Kriegeskorte N, Formisano E, Sorger B, Goebel R. 2007. Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc Natl Acad Sci USA. 104:20600-20605.
44. Kveraga K, Boshyan J, Bar M. 2007. Magnocellular projections as the trigger of top-down facilitation in recognition. J Neurosci. 27:13232-13240.
45. Le Grand R, Mondloch CJ, Maurer D, Brent HP. 2001. Neuroperception. Early visual experience and face processing. Nature. 410:890.
46. Lerner Y, Hendler T, Ben-Bashat D, Harel M, Malach R. 2001. A hierarchical axis of object processing stages in the human visual cortex. Cereb Cortex. 11:287-297.
47. Liu CH, Collin CA, Rainville SJ, Chaudhuri A. 2000. The effects of spatial frequency overlap on face recognition. J Exp Psychol Hum Percept Perform. 26:956-979.
48. Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB. 1995. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA. 92:8135-8139.
49. Marr D. 1982. Vision: a computational investigation into the human representation and processing of visual information. San Francisco (CA): Freeman.
50. Mazer JA, Vinje WE, McDermott J, Schiller PH, Gallant JL. 2002. Spatial frequency and orientation tuning dynamics in area V1. Proc Natl Acad Sci USA. 99:1645-1650.
51. McCarthy G, Puce A, Belger A, Allison T. 1999. Electrophysiological studies of human face perception. II: response properties of face-specific potentials generated in occipitotemporal cortex. Cereb Cortex. 9:431-444. (Pubitemid 29367764)
52. Mihaylova M, Stomonyakov V, Vassilev A. 1999. Peripheral and central delay in processing high spatial frequencies: reaction time and VEP latency studies. Vision Res. 39:699-705.
53. Musselwhite MJ, Jeffreys DA. 1985. The influence of spatial frequency on the reaction times and evoked potentials recorded to grating pattern stimuli. Vision Res. 25:1545-1555.
54. Narayan R, Ergun A, Sen K. 2005. Delayed inhibition in cortical receptive fields and the discrimination of complex stimuli. J Neurophysiol. 94:2970-2975.
55. Nasanen R. 1999. Spatial frequency bandwidth used in the recognition of facial images. Vision Res. 39:3824-3833.
56. Parker DM, Dutch S. 1987. Perceptual latency and spatial frequency. Vision Res. 27:1279-1283.
57. Parker DM, Lishman JR, Hughes J. 1992. Temporal integration of spatially filtered visual images. Perception. 21:147-160.
58. Parker DM, Lishman JR, Hughes J. 1997. Evidence for the view that temporospatial integration in vision is temporally anisotropic. Perception. 26:1169-1180.
59. Peyrin C, Mermillod M, Chokron S, Marendaz C. 2006. Effect of temporal constraints on hemispheric asymmetries during spatial frequency processing. Brain Cogn. 62:214-220.
60. Peyrin C, Michel CM, Schwartz S, Thut G, Seghier M, Landis T, Marendaz C, Vuilleumier P. 2010. The neural substrates and timing of top-down processes during coarse-to-fine categorization of visual scenes: a combined fMRI and ERP study. J Cogn Neurosci.
61. 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.
62. Rajimehr R, Young JC, Tootell RB. 2009. An anterior temporal face patch in human cortex, predicted by macaque maps. Proc Natl Acad Sci USA. 106:1995-2000.
63. Richler JJ, Mack ML, Gauthier I, Palmeri TJ. 2009. Holistic processing of faces happens at a glance. Vision Res. 49:2856-2861.
64. Rolls ET, Baylis GC, Leonard CM. 1985. Role of low and high spatial frequencies in the face-selective responses of neurons in the cortex in the superior temporal sulcus in the monkey. Vision Res. 25:1021-1035.
65. Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E. 2003. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain. 126:2381-2395.
66. Rossion B, Gauthier I, Tarr MJ, Despland P, Bruyer R, Linotte S, Crommelinck M. 2000. The N170 occipito-temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face-specific processes in the human brain. Neuroreport. 11:69-74.
67. Schiltz C, Rossion B. 2006. Faces are represented holistically in the human occipito-temporal cortex. Neuroimage. 32:1385-1394.
68. Schyns PG, Oliva A. 1994. From blobs to boundary edges: evidence for time and spatial scale dependent scene recognition. Psychol Sci. 5:195-200.
69. Sergent J, Ohta S, MacDonald B. 1992. Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain. 115(1):15-36.
70. Sergent J, Signoret JL. 1992. Varieties of functional deficits in prosopagnosia. Cereb Cortex. 2:375-388.
71. Simmons WK, Bellgowan PS, Martin A. 2007. Measuring selectivity in fMRI data. Nat Neurosci. 10:4-5.
72. Singer JM, Sheinberg DL. 2006. Holistic processing unites face parts across time. Vision Res. 46:1838-1847.
73. Sripati AP, Olson CR. 2009. Representing the forest before the trees: a global advantage effect in monkey inferotemporal cortex. J Neurosci. 29:7788-7796.
74. Sripati AP, Yoshioka T, Denchev P, Hsiao SS, Johnson KO. 2006. Spatiotemporal receptive fields of peripheral afferents and cortical area 3b and 1 neurons in the primate somatosensory system. J Neurosci. 26:2101-2114.
75. Sugase Y, Yamane S, Ueno S, Kawano K. 1999. Global and fine information coded by single neurons in the temporal visual cortex. Nature. 400:869-873.
76. Talairach G, Tournoux P. 1988. Coplanar stereotaxic atlas of the human brain. New York: Thieme.
77. Tanskanen T, Nasanen R, Montez T, Paallysaho J, Hari R. 2005. Face recognition and cortical responses show similar sensitivity to noise spatial frequency. Cereb Cortex. 15:526-534.
78. Tolhurst DJ, Tadmor Y, Chao T. 1992. Amplitude spectra of natural images. Ophthal Physiol Opt. 12:229-232.
79. Vlamings PH, Goffaux V, Kemner C. 2009. Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information? J Vis. 9(12):11-13.
80. Vuilleumier P, Armony JL, Driver J, Dolan RJ. 2003. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci. 6:624-631.
81. Watt RJ. 1987. Scanning from coarse to fine spatial scales in the human visual system after the onset of a stimulus. J Opt Soc Am A. 4:2006-2021.
82. Williams NR, Willenbockel V, Gauthier I. 2009. Sensitivity to spatial frequency and orientation content is not specific to face perception. Vision Res. 49:2353-2362.
83. Yue X, Tjan BS, Biederman I. 2006. What makes faces special? Vision Res. 46:3802-3811.