Investigating representations of facial identity in human ventral visual cortex with transcranial magnetic stimulation

Frontiers in Human Neuroscience

Volumn 4, Issue , 2010, Pages

  Gilaie Dotan, Sharon ^a,b   Silvanto, Juha ^a,c   Schwarzkopf, Dietrich S ^a,b   Rees, Geraint ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c AALTO UNIVERSITY   (Finland)

Author keywords

Faces; Familiar; Famous; Identity; Lo; OfA; State dependent Tms

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN REGION; CONTROLLED STUDY; DECISION MAKING; EVOKED RESPONSE; FACE PROFILE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAIR COLOR; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; MALE; MENTAL TASK; NERVE FUNCTION; NEUROIMAGING; NEUROMODULATION; NORMAL HUMAN; OCCIPITAL CORTEX; PATTERN RECOGNITION; REACTION TIME; REPEAT PROCEDURE; SKIN COLOR; TASK PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL STIMULATION;

EID: 78549262412     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2010.00050     Document Type: Article

References (63)

1. Andrews, T. J., and Ewbank, M. P. (2004). Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage 23, 905-913.
2. Avidan, G., Harel, M., Hendler, T., Ben-Bashat, D., Zohary, E., and Malach, R. (2002a). Contrast sensitivity in human visual areas and its relationship to object recognition. J. Neurophysiol. 87, 3102-3116.
3. Avidan, G., Hasson, U., Hendler, T., Zohary, U., and Malach, R. (2002b). Analysis of the neuronal selectivity underlying low fMRI signals. Curr. Biol. 12, 964-972.
4. Bart, E., and Ullman, S. (2008). Class-based feature matching across unrestricted transformations. IEEE Trans. Pattern Anal. Mach. Intell. 30, 1618-1631.
5. Campana, G., Cowey, A., and Walsh, V. (2002). Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb. Cortex 12, 663-669.
6. Cattaneo, Z., Devlin, J. T., Salvini, F., Vecchi, T., and Silvanto, J. (2010). The causal role of category-specific neuronal representations in the left ventral premotor cortex (PMv) in semantic processing. Neuroimage 49, 2728-2734.
7. Cattaneo, Z., Vecchi, T., Pascual-Leone, A., and Silvanto, J. (2009). Contrasting early visual cortical activation states causally involved in visual imagery and short-term memory. Eur. J. Neurosci. 30, 1393-1400.
8. Chen, C. C., Kao, K. L., and Tyler, C. W. (2007). Face configuration processing in the human brain: the role of symmetry. Cereb. Cortex 17, 1423-1432.
9. Cohen Kadosh, R., Muggleton, N., Silvanto, J., and Walsh, V. (2010). Double dissociation of format-dependent and number-specific neurons in human parietal cortex. Cereb. Cortex. doi: 10.1093/cercor/bHp273. [Epub ahead of print].
10. Dakin, S. C., and Watt, R. J. (2009). Biological "bar codes" in human faces. J. Vision 9, 1-10.
11. Fang, F., Murray, S. O., and He, S. (2007). Duration-dependent FMRI adaptation and distributed viewer-centered face representation in human visual cortex. Cereb. Cortex 17, 1402-1411.
12. Gauthier, I., Skudlarski, P., Gore, J. C., and Anderson, A. W. (2000a). Expertise for cars and birds recruits brain areas involved in face recognition. Nat. Neurosci. 3, 191-197.
13. Gauthier, I., Tarr, M. J., Moylan, J., Skudlarski, P., Gore, J. C., and Anderson, A. W. (2000b). The fusiform "face area" is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 12, 495-504.
14. Gilaie-Dotan, S., Gelbard-Sagiv, H., and Malach, R. (2010). Perceptual shape sensitivity to upright and inverted faces is reflected in neuronal adaptation. Neuroimage 50, 383-395.
15. Gilaie-Dotan, S., and Malach, R. (2007). Sub-exemplar shape tuning in human face-related areas. Cereb. Cortex 17, 325-338.
16. Gilaie-Dotan, S., Nir, Y., and Malach, R. (2008). Regionally-specific adaptation dynamics in human object areas. Neuroimage 39, 1926-1937.
17. Grill-Spector, K., Kushnir, T., Edelman, S., Itzchak, Y., and Malach, R. (1998a). Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21, 191-202.
18. Grill-Spector, K., Kushnir, T., Hendler, T., Edelman, S., Itzchak, Y., and Malach, R. (1998b). A sequence of object-processing stages revealed by fMRI in the human occipital lobe. Hum. Brain Mapp. 6, 316-328.
19. Grosbras, M. H., and Paus, T. (2003). Transcranial magnetic stimulation of the human frontal eye field facilitates visual awareness. Eur. J. Neurosci. 18, 3121-3126.
20. Grossman, E. D., and Blake, R. (2002). Brain areas active during visual perception of biological motion. Neuron 35, 1167-1175.
21. Halgren, E., Dale, A. M., Sereno, M. I., Tootell, R. B. H., Marinkovic, K., and Rosen, B. R. (1999). Location of human face-selective cortex with respect to retinotopic areas. Hum. Brain Mapp. 7, 29-37.
22. Hancock, P. J., Bruce, V. V., and Burton, A. M. (2000). Recognition of unfamiliar faces. Trends Cogn. Sci. 4, 330-337.
23. Hasson, U., Harel, M., Levy, I., and Malach, R. (2003). Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37, 1027-1041.
24. Haxby, J. V., Hoffman, E. A., and Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223-233.
25. Haxby, J. V., Ungerleider, L. G., Clark, V. P., Schouten, J. L., Hoffman, E. A., and Martin, A. (1999). The effect of face inversion on activity in human neural systems for face and object perception. Neuron 22, 189-199.
26. Hilgetag, C. C., Theoret, H., and Pascual-Leone, A. (2001). Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex. Nat. Neurosci. 4, 953-957.
27. Johnston, R. A., and Barry, C. (2001). Best face forward: similarity effects in repetition priming of face recognition. Q. J. Exp. Psychol. A 54, 383-396.
28. Kanwisher, N., McDermott, J., and Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302-4311.
29. Kriegeskorte, N., Formisano, E., Sorger, B., and Goebel, R. (2007). Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc. Natl. Acad. Sci. U.S.A. 104, 20600-20605.
30. Kristjansson, A., and Campana, G. (2010). Where perception meets memory: a review of repetition priming in visual search tasks. Atten. Percept. Psychophys. 72, 5-18.
31. Lerner, Y., Epshtein, B., Ullman, S., and Malach, R. (2008). Class information predicts activation by object fragments in human object areas. J. Cogn. Neurosci. 20, 1189-1206.
32. Lerner, Y., Hendler, T., Ben-Bashat, D., Harel, M., and Malach, R. (2001). A hierarchical axis of object processing stages in the human visual cortex. Cereb. Cortex 11, 287-297.
33. Levy, I., Hasson, U., Avidan, G., Hendler, T., and Malach, R. (2001). Center-periphery organization of human object areas. Nat. Neurosci. 4, 533-539.
34. Levy, I., Hasson, U., and Malach, R. (2004). One picture is worth at least a million neurons. Curr. Biol. 14, 996-1001.
35. Liu, J., Harris, A., and Kanwisher, N. (2009). Perception of face parts and face configurations: an fMRI study. J. Cogn. Neurosci. 22, 203-211.
36. 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., and Tootell, R. B. (1995). Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl. Acad. Sci. U.S.A. 92, 8135-8139.
37. McCarthy, G., Puce, A., Gore, J. C., and Allison, T. (1997). Face specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605-610.
38. McKone, E. (2008). Configural processing and face viewpoint. J. Exp. Psychol. Hum. Percept. Perform. 34, 310-327.
39. Newell, F. N., Chiroro, P., and Valentine, T. (1999). Recognizing unfamiliar faces: the effects of distinctiveness and view. Q. J. Exp. Psychol. A 52, 509-534.
40. Pitcher, D., Charles, L., Devlin, J. T., Walsh, V., and Duchaine, B. (2009). Triple dissociation of faces, bodies, and objects in extrastriate cortex. Curr. Biol. 19, 319-324.
41. Pitcher, D., Garrido, L., Walsh, V., and Duchaine, B. C. (2008). Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. J. Neurosci. 28, 8929-8933.
42. Pitcher, D., Walsh, V., Yovel, G., and Duchaine, B. (2007). TMS evidence for the involvement of the right occipital face area in early face processing. Curr. Biol. 17, 1568-1573.
43. Pourtois, G., Schwartz, S., Seghier, M. L., Lazeyras, F., and Vuilleumier, P. (2005). Portraits or people? Distinct representations of face identity in the human visual cortex. J. Cogn. Neurosci. 17, 1043-1057.
44. Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., and Fried, I. (2005). Invariant visual representation by single neurons in the human brain. Nature 435, 1102-1107.
45. Rhodes, G., Michie, P. T., Hughes, M. E., and Byatt, G. (2009). The fusiform face area and occipital face area show sensitivity to spatial relations in faces. Eur. J. Neurosci. 30, 721-733.
46. Rolls, E. T. (2007). The representation of information about faces in the temporal and frontal lobes. Neuropsychologia 45, 124-143.
47. Rossion, B., Caldara, R., Seghier, M., Schuller, A. M., Lazeyras, F., and Mayer, E. (2003). A network of occipito-temHancock poral face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126, 2381-2395.
48. Rotshtein, P., Geng, J. J., Driver, J., and Dolan, R. J. (2007). Role of features and second-order spatial relations in face discrimination, face recognition, and individual face skills: behavioral and functional magnetic resonance imaging data. J. Cogn. Neurosci. 19, 1435-1452.
49. Rotshtein, P., Henson, R. N., Treves, A., Driver, J., and Dolan, R. J. (2005). Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat. Neurosci. 8, 107-113.
50. Silvanto, J., Lavie, N., and Walsh, V. (2005). Double dissociation of V1 and V5/MT activity in visual awareness. Cereb. Cortex 15, 1736-1741.
51. Silvanto, J., and Muggleton, N. G. (2008a). New light through old windows: moving beyond the "virtual lesion" approach to transcranial magnetic stimulation. Neuroimage 39, 549-552.
52. Silvanto, J., and Muggleton, N. G. (2008b). A novel approach for enhancing the functional specificity of TMS: revealing the properties of distinct neural populations within the stimulated region. Clin. Neurophysiol. 119, 724-726.
53. Silvanto, J., Muggleton, N., and Walsh, V. (2008). State-dependency in brain stimulation studies of perception and cognition. Trends Cogn. Sci. 12, 447-454.
54. Silvanto, J., Schwarzkopf, D. S., Gilaie-Dotan, S., and Rees, G. (in press). Differing causal roles for LO and OFA in invariant shape recognition. Eur. J. Neurosci.
55. Steeves, J., Dricot, L., Goltz, H. C., Sorger, B., Peters, J., Milner, A. D., Goodale, M. A., Goebel, R., and Rossion, B. (2009). Abnormal face identity coding in the middle fusiform gyrus of two brain-damaged prosopagnosic patients. Neuropsychologia 47, 2584-2592.
56. Steeves, J. K., Culham, J. C., Duchaine, B. C., Pratesi, C. C., Valyear, K. F., Schindler, I., Humphrey, G. K., Milner, A. D., and Goodale, M. A. (2006). The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 44, 594-609.
57. Topper, R., Mottaghy, F. M., Brugmann, M., Noth, J., and Huber, W. (1998). Facilitation of picture naming by focal transcranial magnetic stimulation of Wernicke's area. Exp. Brain Res. 121, 371-378.
58. Ullman, S., and Bart, E. (2004). Recognition invariance obtained by extended and invariant features. Neural Netw. 17, 833-848.
59. Ullman, S., Vidal-Naquet, M., and Sali, E. (2002). Visual features of intermediate complexity and their use in classification. Nat. Neurosci. 5, 682-687.
60. Viskontas, I. V., Quiroga, R. Q., and Fried, I. (2009). Human medial temporal lobe neurons respond preferentially to personally relevant images. Proc. Natl. Acad. Sci. U.S.A. 106, 21329-21334.
61. Walsh, V., Ellison, A., Battelli, L., and Cowey, A. (1998). Task-specific impairments and enhancements induced by magnetic stimulation of human visual area V5. Proc. R. Soc. Lond., B, Biol. Sci. 265, 537-543.
62. Winston, J. S., Henson, R. N., Fine-Goulden, M. R., and Dolan, R. J. (2004). fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J. Neurophysiol. 92, 1830-1839.
63. Yovel, G., and Kanwisher, N. (2005). The neural basis of the behavioral face-inversion effect. Curr. Biol. 15, 2256-2262.