Perceptual shape sensitivity to upright and inverted faces is reflected in neuronal adaptation

NeuroImage

Volumn 50, Issue 2, 2010, Pages 383-395

  Gilaie Dotan, Sharon ^a,b,c   Gelbard Sagiv, Hagar ^a   Malach, Rafael ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Face perception; fMRI; Human cortex; Object recognition; Ventral stream

Indexed keywords

ADAPTATION; ADULT; ARTICLE; BEHAVIOR; BRAIN CORTEX; CONTROLLED STUDY; CORRELATION ANALYSIS; FACE; FEMALE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MORPHOLOGY; NEUROIMAGING; NORMAL HUMAN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; RECOGNITION; SENSITIVITY ANALYSIS; SUBICULUM; BRAIN MAPPING; COMPUTER ASSISTED DIAGNOSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ADULT; BRAIN MAPPING; CEREBRAL CORTEX; DISCRIMINATION (PSYCHOLOGY); FACE; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; PATTERN RECOGNITION, VISUAL; RECOGNITION (PSYCHOLOGY); YOUNG ADULT;

EID: 77952301711     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.12.077     Document Type: Article

References (62)

1. Aguirre, G.K., Zarahn, E., D'Esposito, M., 1998. An area within human ventral cortex sensitive to "building" stimuli: evidence and implications. Neuron 21, 373-383.
2. Aguirre, G.K., Singh, R., D'Esposito, M., 1999. Stimulus inversion and the responses of face and object-sensitive cortical areas. NeuroReport 10, 189-194.
3. Allison, T., Ginter, H., McCarthy, G., Nobre, A.C., Puce, A., Luby, M., Spencer, D.D., 1994. Face recognition in human extrastriate cortex. J. Neurophysiol. 71, 821-825.
4. Avidan, G., Harel, M., Hendler, T., Ben-Bashat, D., Zohary, E., Malach, R., 2002a. Contrast sensitivity in human visual areas and its relationship to object recognition. J. Neurophysiol. 87, 3102-3116.
5. Avidan, G., Hasson, U., Hendler, T., Zohary, U., Malach, R., 2002b. Analysis of the neuronal selectivity underlying low fMRI signals. Curr. Biol. 12, 964-972.
6. Bitterman, Y., Mukamel, R., Malach, R., Fried, I., Nelken, I., 2008. Ultra-ne frequency tuning revealed in single neurons of human auditory cortex. Nature 451, 197-201.
7. Bruce, V., Doyle, T., Dench, N., Burton, M., 1991. Remembering facial congurations. Cognition 38, 109-144.
8. Cox, R., 1996. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173.
9. Epstein, R., Kanwisher, N., 1998. A cortical representation of the local visual environment. Nature 392, 598-601.
10. Epstein, R.A., Higgins, J.S., Parker, W., Aguirre, G.K., Cooperman, S., 2006. Cortical correlates of face and scene inversion: a comparison. Neuropsychologia 44, 1145-1158.
11. Fang, F., Murray, S.O., He, S., 2007. Duration-dependent fMRI adaptation and distributed viewer-centered face representation in human visual cortex. Cereb. Cortex 17, 1402-1411.
12. Farah, M.J., 1996. Is face recognition 'special'? Evidence from neuropsychology. Behav. Brain. Res. 76, 181-189.
13. Farah, M.J., Tanaka, J.W., Drain, H.M., 1995. What causes the face inversion effect? J. Exp. Psychol. Hum. Percept. Perform. 21, 628-634.
14. Farah, M.J., Wilson, K.D., Drain, M., Tanaka, J.N., 1998. What is "special" about face perception? Psychol. Rev. 105, 482-498.
15. Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., Noll, D.C., 1995. Improved assessment of signicant activation in functional magnetic-resonance-imaging (fMRI)-use of a cluster-size threshold. Magn. Reson. Med. 33, 636-647.
16. Fox, C.J., Moon, S.Y., Iaria, G., Barton, J.J., 2009. The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. NeuroImage 44, 569-580.
17. Freiwald, W.A., Tsao, D.Y., Livingstone, M.S., 2009. A face feature space in the macaque temporal lobe. Nat. Neurosci. 12, 1187-1196.
18. Friston, J., Homes, A., Worsley, K., Poline, J., Frith, C., Frackwowiak, R., 1994. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain. Mapp. 2, 189-210.
19. Friston, K.J., Holmes, A.P., Price, C.J., Buchel, C., Worsley, K.J., 1999. Multisubject fMRI studies and conjunction analyses. NeuroImage 10, 385-396.
20. Georgopoulos, A.P., Schwartz, A.B., Kettner, R.E., 1986. Neuronal population coding of movement direction. Science 233, 1416-1419.
21. Gilaie-Dotan, S., Malach, R., 2007. Sub-exemplar shape tuning in human face-related areas. Cereb. Cortex. 17, 325-338.
22. Goffaux, V., Rossion, B., 2007. Face inversion disproportionately impairs the perception of vertical but not horizontal relations between features. J.Exp. Psychol.:. Hum. Percept. Perform. 33, 995-1002.
23. Grill-Spector, K., 2003. The neural basis of object perception. Curr. Opin. Neurobiol. 13, 159-166.
24. Grill-Spector, K., Malach, R., 2001. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta. Psychol. (Amst). 107, 293-321.
25. Grill-Spector, K., Kushnir, T., Hendler, T., Edelman, S., Itzchak, Y., Malach, R., 1998. A sequence of object-processing stages revealed by fMRI in the human occipital lobe. Hum. Brain. Mapp. 6, 316-328.
26. Grill-Spector, K., Kourtzi, Z., Kanwisher, N., 2001. The lateral occipital complex and its role in object recognition. Vision. Res. 41, 1409-1422.
27. Hasson, U., Harel, M., Levy, I., Malach, R., 2003. Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37, 1027-1041.
28. Haxby, J.V., Ungerleider, L.G., Clark, V.P., Schouten, J.L., Hoffman, E.A., Martin, A., 1999. The effect of face inversion on activity in human neural systems for face and object perception. Neuron 22, 189-199.
29. Ishai, A., Ungerleider, L.G., Martin, A., Schouten, H.L., Haxby, J.V., 1999. Distributed representation of objects in the human ventral visual pathway. Proc. Natl. Acad. Sci. USA. 96, 9379-9384.
30. Jazayeri, M., Movshon, J.A., 2006. Optimal representation of sensory information by neural populations. Nat. Neurosci. 9, 690-696.
31. Jiang, X., Rosen, E., Zefro, T., Vanmeter, J., Blanz, V., Riesenhuber, M., 2006. Evaluation of a shape-based model of human face discrimination using fMRI and behavioral techniques. Neuron 50, 159-172.
32. Kanwisher, N., McDermott, J., Chun, M.M., 1997. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302-4311.
33. Kanwisher, N., Tong, F., Nakayama, K., 1998. The effect of face inversion on the human fusiform face area. Cognition 68, B1-11.
34. Leopold, D.A., O'Toole, A.J., Vetter, T., Blanz, V., 2001. Prototype-referenced shape encoding revealed by high-level aftereffects. Nat. Neurosci. 4, 89-94.
35. Leopold, D.A., Bondar, I.V., Giese, M.A., 2006. Norm-based face encoding by single neurons in the monkey inferotemporal cortex. Nature 442, 572-575.
36. Lerner, Y., Epshtein, B., Ullman, S., Malach, R., 2008. Class information predicts activation by object fragments in human object areas. J. cogn. Neurosci. 20, 1189-1206.
37. Levy, I., Hasson, U., Avidan, G., Hendler, T., Malach, R., 2001. Center-periphery organization of human object areas. Nat. Neurosci. 4, 533-539.
38. Levy, I., Hasson, U., Harel, M., Malach, R., 2004a. Functional analysis of the periphery effect in human building related areas. Hum. Brain. Mapp. 22, 15-26.
39. Levy, I., Hasson, U., Malach, R., 2004b. One picture is worth at least a million neurons. Curr. Biol. 14, 996-1001.
40. Liu, Y., Murray, S.O., Jagadeesh, B., 2009. Time course and stimulus dependence of repetition-induced response suppression in inferotemporal cortex. J. Neurophysiol. 101, 418-436.
41. Malach, R., Reppas, J.B., Benson, R.R., Kwong, K.K., Jiang, H., Kennedy, W.A., Ledden, P.J., Brady, T.J., Rosen, B.R., Tootell, R.B., 1995. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl. Acad. Sci. USA. 92, 8135-8139.
42. Martinez, A., and Benavente, R. (1998). The AR Face Database. CVC Technical Report #24.
43. Mazard, A., Schiltz, C., Rossion, B., 2006. Recovery from adaptation to facial identity is larger for upright than inverted faces in the human occipito-temporal cortex. Neuropsychologia 44, 912-922.
44. McKone, E., Kanwisher, N., Duchaine, B.C., 2007. Can generic expertise explain special processing for faces? Trends. Cogn. Sci. 11, 8-15.
45. McMahon, D.B., Olson, C.R., 2007. Repetition suppression in monkey inferotemporal cortex: relation to behavioral priming. J. Neurophysiol. 97, 3532-3543.
46. Murray, J.E., Yong, E., Rhodes, G., 2000. Revisiting the perception of upside-down faces. Psychol. Sci. 11, 492-496.
47. Puce, A., Allison, T., Gore, J.C., McCarthy, G., 1995. Face-sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol. 74, 1192-1199.
48. Rhodes, G., Jeffery, L., 2006. Adaptive norm-based coding of facial identity. Vision Res. 46, 2977-2987.
49. Rhodes, G., Brake, S., Atkinson, A.P., 1993. What's lost in inverted faces? Cognition 47, 25-57.
50. Rossion, B., Gauthier, I., 2002. How does the brain process upright and inverted faces? Behav. Cogn. Neurosci. Rev. 1, 63-75.
51. Rotshtein, P., Henson, R.N., Treves, A., Driver, J., Dolan, R.J., 2004. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat. Neurosci.
52. Sawamura, H., Orban, G.A., Vogels, R., 2006. Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the fMRI adaptation paradigm. Neuron 49, 307-318.
53. Sereno, M.I., Dale, A.M., Reppas, J.B., Kwong, K.K., Belliveau, J.W., Brady, T.J., Rosen, B.R., Tootell, R.B., 1995. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889-893.
54. Talairach, J., Tournoux, P., 1988. Co-Planar Stereotaxic Atlas of the Human Brain. Thieme Medical Publishers, New York.
55. Tanaka, K., 1996. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109-139.
56. Tootell, R.B., Dale, A.M., Sereno, M.I., Malach, R., 1996. New images from human visual cortex. Trends. Neurosci. 19, 481-489.
57. Valentine, T., 1988. Upside-down faces: a review of the effect of inversion upon face recognition. Br. J. Psychol. 79 (Pt 4), 471-491.
58. Valentine, T., Endo, M., 1992. Towards an exemplar model of face processing: the effects of race and distinctiveness. Q. J. Exp. Psychol. A. 44, 671-703.
59. Verhoef, B.E., Kayaert, G., Franko, E., Vangeneugden, J., Vogels, R., 2008. Stimulus similarity-contingent neural adaptation can be time and cortical area dependent. J. Neurosci. 28, 10631-10640.
60. Welchman, A.E., Deubelius, A., Conrad, V., Bulthoff, H.H., Kourtzi, Z., 2005. 3D shape perception from combined depth cues in human visual cortex. Nat. Neurosci. 8, 820-827.
61. Yin, R.K. (1969). Looking at upside-down faces. Looking at upside-down faces 81, 141-145.
62. Yovel, G., Kanwisher, N., 2005. The neural basis of the behavioral face-inversion effect. Curr. Biol. 15, 2256-2262.