Individual differences in cortical face selectivity predict behavioral performance in face recognition

Frontiers in Human Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Huang, Lijie ^a   Song, Yiying ^a   Li, Jingguang ^a   Zhen, Zonglei ^a   Yang, Zetian ^a   Liu, Jia ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Face recognition; Functional magnetic resonance imaging; Fusiform face area; Individual differences; Object selectivity

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BEHAVIOR; BRAIN REGION; COLLEGE STUDENT; CONTROLLED STUDY; CORTICAL FACE SELECTIVITY; FACE PROFILE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; OCCIPITAL CORTEX; PATTERN RECOGNITION; RELIABILITY; STIMULUS RESPONSE; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; VISUAL STIMULATION; YOUNG ADULT;

EID: 84903717538     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00483     Document Type: Article

References (75)

1. Allison, T., Puce, A., and McCarthy, G. (2000). Social perception from visual cues: role of the STS region. Trends Cogn. Sci. 4, 267-278. doi: 10.1016/S1364-6613(00)01501-1
2. 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. doi: 10.1016/j.neuroimage.2004.07.060
3. Andrews, T. J., Schluppeck, D., Homfray, D., Matthews, P., and Blakemore, C. (2002). Activity in the fusiform gyrus predicts conscious perception of Rubin's vase-face illusion. Neuroimage 17, 890-901. doi: 10.1006/nimg.2002.1243
4. Avidan, G., and Behrmann, M. (2009). Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Curr. Biol. 19, 1146-1150. doi: 10.1016/j.cub.2009.04.060
5. Avidan, G., Tanzer, M., Hadj-Bouziane, F., Liu, N., Ungerleider, L. G., and Behrmann, M. (2013). Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. Cereb. Cortex 24, 1565-1578. doi: 10.1093/cercor/bht007
6. Barton, J. J., Press, D. Z., Keenan, J. P., and O'Connor, M. (2002). Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia. Neurology 58, 71-78. doi: 10.1212/WNL.58.1.71
7. Behrmann, M., and Avidan, G. (2005). Congenital prosopagnosia: face-blind from birth. Trends Cogn. Sci. 9, 180-187. doi: 10.1016/j.tics.2005.02.011
8. Behrmann, M., Avidan, G., Gao, F., and Black, S. (2007). Structural imaging reveals anatomical alterations in inferotemporal cortex in congenital prosopagnosia. Cereb. Cortex 17, 2354-2363. doi: 10.1093/cercor/bhl144
9. Behrmann, M., Avidan, G., Marotta, J. J., and Kimchi, R. (2005). Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. J. Cogn. Neurosci. 17, 1130-1149. doi: 10.1162/0898929054475154
10. Busigny, T., Graf, M., Mayer, E., and Rossion, B. (2010). Acquired prosopagnosia as a face-specific disorder: ruling out the general visual similarity account. Neuropsychologia 48, 2051-2067. doi: 10.1016/j.neuropsychologia.2010.03.026
11. Calder, A. J., and Young, A. W. (2005). Understanding the recognition of facial identity and facial expression. Nat. Rev. Neurosci. 6, 641-651. doi: 10.1038/nrn1724
12. Carey, S., and Diamond, R. (1977). From piecemeal to configurational representation of faces. Science 195, 312-314. doi: 10.1126/science.831281
13. Cohen, L., Dehaene, S., Naccache, L., Lehericy, S., Dehaene-Lambertz, G., Henaff, M. A., et al. (2000). The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 123(Pt 2), 291-307. doi: 10.1093/brain/123.2.291
14. Damasio, A. R., Damasio, H., and Van Hoesen, G. W. (1982). Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32, 331-341. doi: 10.1212/WNL.32.4.331
15. DeGutis, J. M., Bentin, S., Robertson, L. C., and D'Esposito, M. (2007). Functional plasticity in ventral temporal cortex following cognitive rehabilitation of a congenital prosopagnosic. J. Cogn. Neurosci. 19, 1790-1802. doi: 10.1162/jocn.2007.19.11.1790
16. Dehaene, S., Pegado, F., Braga, L. W., Ventura, P., Nunes Filho, G., Jobert, A., et al. (2010). How learning to read changes the cortical networks for vision and language. Science 330, 1359-1364. doi: 10.1126/science.1194140
17. Diamond, R., and Carey, S. (1986). Why faces are and are not special: an effect of expertise. J. Exp. Psychol. Gen. 115, 107-117. doi: 10.1037//0096-3445.115.2.107
18. Dinkelacker, V., Gruter, M., Klaver, P., Gruter, T., Specht, K., Weis, S., et al. (2011). Congenital prosopagnosia: multistage anatomical and functional deficits in face processing circuitry. J. Neurol. 258, 770-782. doi: 10.1007/s00415-010-5828-5
19. Downing, P. E., Jiang, Y., Shuman, M., and Kanwisher, N. (2001). A cortical area selective for visual processing of the human body. Science 293, 2470-2473. doi: 10.1126/science.1063414
20. Duchaine, B. C., and Nakayama, K. (2006). Developmental prosopagnosia: a window to content-specific face processing. Curr. Opin. Neurobiol. 16, 166-173. doi: 10.1016/j.conb.2006.03.003
21. Epstein, R., and Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature 392, 598-601. doi: 10.1038/33402
22. Fox, C. J., Moon, S. Y., Iaria, G., and 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. doi: 10.1016/j.neuroimage.2008.09.011
23. Furl, N., Garrido, L., Dolan, R. J., Driver, J., and Duchaine, B. (2011). Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. J. Cogn. Neurosci. 23, 1723-1740. doi: 10.1162/jocn.2010.21545
24. Garrido, L., Furl, N., Draganski, B., Weiskopf, N., Stevens, J., Tan, G. C., et al. (2009). Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics. Brain 132(Pt 12), 3443-3455. doi: 10.1093/brain/awp271
25. Gauthier, I., Behrmann, M., and Tarr, M. J. (1999). Can face recognition really be dissociated from object recognition? J. Cogn. Neurosci. 11, 349-370. doi: 10.1162/089892999563472
26. Gauthier, I., Tarr, M. J., Moylan, J., Skudlarski, P., Gore, J. C., and Anderson, A. W. (2000). The fusiform "face area" is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 12, 495-504. doi: 10.1162/089892900562165
27. Goesaert, E., and Op de Beeck, H. P. (2013). Representations of facial identity information in the ventral visual stream investigated with multivoxel pattern analyses. J. Neurosci. 33, 8549-8558. doi: 10.1523/JNEUROSCI.1829-12.2013
28. Golarai, G., Ghahremani, D. G., Whitfield-Gabrieli, S., Reiss, A., Eberhardt, J. L., Gabrieli, J. D., et al. (2007). Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat. Neurosci. 10, 512-522. doi: 10.1038/nn1865
29. Grill-Spector, K., Knouf, N., and Kanwisher, N. (2004). The fusiform face area subserves face perception, not generic within-category identification. Nat. Neurosci. 7, 555-562. doi: 10.1038/nn1224
30. Grill-Spector, K., Kushnir, T., Hendler, T., and Malach, R. (2000). The dynamics of object-selective activation correlate with recognition performance in humans. Nat. Neurosci. 3, 837-843. doi: 10.1038/77754
31. Hadjikhani, N., and de Gelder, B. (2002). Neural basis of prosopagnosia: an fMRI study. Hum. Brain Mapp. 16, 176-182. doi: 10.1002/hbm.10043
32. Hao, X., Wang, K., Li, W., Yang, W., Wei, D., Qiu, J., et al. (2013). Individual differences in brain structure and resting brain function underlie cognitive styles: evidence from the embedded figures test. PLoS ONE 8:e78089. doi: 10.1371/journal.pone.0078089
33. Hasson, U., Avidan, G., Deouell, L. Y., Bentin, S., and Malach, R. (2003). Face-selective activation in a congenital prosopagnosic subject. J. Cogn. Neurosci. 15, 419-431. doi: 10.1162/089892903321593135
34. Hasson, U., Hendler, T., Ben Bashat, D., and Malach, R. (2001). Vase or face? A neural correlate of shape-selective grouping processes in the human brain. J. Cogn. Neurosci. 13, 744-753. doi: 10.1162/08989290152541412
35. 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. doi: 10.1016/S1364-6613(00)01482-0
36. He, Q., Xue, G., Chen, C., Lu, Z. L., and Dong, Q. (2013). Decoding the neuroanatomical basis of reading ability: a multivoxel morphometric study. J. Neurosci. 33, 12835-12843. doi: 10.1523/JNEUROSCI.0449-13.2013
37. Hoffman, E. A., and Haxby, J. V. (2000). Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nat. Neurosci. 3, 80-84. doi: 10.1038/71152
38. Holmes, A. J., Lee, P. H., Hollinshead, M. O., Bakst, L., Roffman, J. L., Smoller, J. W., et al. (2012). Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. J. Neurosci. 32, 18087-18100. doi: 10.1523/JNEUROSCI.2531-12.2012
39. Kanwisher, N. (2000). Domain specificity in face perception. Nat. Neurosci. 3, 759-763. doi: 10.1038/77664
40. Kanwisher, N. (2003). "The ventral visual pathway in humans: evidence from fMRI, " in The Visual Neurosciences, ed L. Chalupa and J. Werner (Cambridge, MA: MIT Press), 1179-1189.
41. 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.
42. Kress, T., and Daum, I. (2003). Developmental prosopagnosia: a review. Behav. Neurol. 14, 109-121. doi: 10.1155/2003/520476
43. Minnebusch, D. A., Suchan, B., Koster, O., and Daum, I. (2009). A bilateral occipitotemporal network mediates face perception. Behav. Brain Res. 198, 179-185. doi: 10.1016/j.bbr.2008.10.041
44. Moscovitch, M., Winocur, G., and Behrmann, M. (1997). What is special about face recognition? nineteen experiments on a person with visual object agnosia and dyslexia but normal face recognition. J. Cogn. Neurosci. 9, 555-604. doi: 10.1162/jocn.1997.9.5.555
45. Nestor, A., Plaut, D. C., and Behrmann, M. (2011). Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis. Proc. Natl. Acad. Sci. U.S.A. 108, 9998-10003. doi: 10.1073/pnas.1102433108
46. Pashler, H., and Harris, C. R. (2012). Is the replicability crisis overblown? Three arguments examined. Perspect. Psychol. Sci. 7, 531-536. doi: 10.1177/1745691612463401
47. Pinsk, M. A., Arcaro, M., Weiner, K. S., Kalkus, J. F., Inati, S. J., Gross, C. G., et al. (2009). Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. J. Neurophysiol. 101, 2581-2600. doi: 10.1152/jn.91198.2008
48. 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. doi: 10.1016/j.cub.2009.01.007
49. Pitcher, D., Dilks, D. D., Saxe, R. R., Triantafyllou, C., and Kanwisher, N. (2011). Differential selectivity for dynamic versus static information in face-selective cortical regions. Neuroimage 56, 2356-2363. doi: 10.1016/j.neuroimage.2011.03.067
50. Rehnman, J., and Herlitz, A. (2007). Women remember more faces than men do. Acta Psychol. (Amst) 124, 344-355. doi: 10.1016/j.actpsy.2006.04.004
51. Rossion, B. (2008). Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. Neuroimage 40, 423-426. doi: 10.1016/j.neuroimage.2007.10.047
52. Rossion, B., Caldara, R., Seghier, M., Schuller, A. M., Lazeyras, F., and 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(Pt 11), 2381-2395. doi: 10.1093/brain/awg241
53. 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. doi: 10.1038/nn1370
54. Saygin, Z. M., Osher, D. E., Koldewyn, K., Reynolds, G., Gabrieli, J. D., and Saxe, R. R. (2012). Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat. Neurosci. 15, 321-327. doi: 10.1038/nn.3001
55. Schiltz, C., Sorger, B., Caldara, R., Ahmed, F., Mayer, E., Goebel, R., et al. (2006). Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in the right middle fusiform gyrus. Cereb. Cortex 16, 574-586. doi: 10.1093/cercor/bhj005
56. Schmidt, F. L., and Hunter, J. E. (1999). Theory testing and measurement error. Intelligence 27, 183-198. doi: 10.1016/S0160-2896(99)00024-0
57. Sergent, J., and Signoret, J. L. (1992). Varieties of functional deficits in prosopagnosia. Cereb. Cortex. 2, 375-388. doi: 10.1093/cercor/2.5.375
58. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl. 1), S208-S219. doi: 10.1016/j.neuroimage.2004.07.051
59. Sommer, W., Hildebrandt, A., Kunina-Habenicht, O., Schacht, A., and Wilhelm, O. (2013). Sex differences in face cognition. Acta Psychol. (Amst) 142, 62-73. doi: 10.1016/j.actpsy.2012.11.001
60. Tanaka, J. W., and Farah, M. J. (1993). Parts and wholes in face recognition. Q. J. Exp. Psychol. A 46, 225-245. doi: 10.1080/14640749308401045
61. Thomas, C., Avidan, G., Humphreys, K., Jung, K. J., and Behrmann, M. (2009). Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia. Nat. Neurosci. 12, 29-31. doi: 10.1038/nn.2224
62. Tong, F., Nakayama, K., Vaughan, J. T., and Kanwisher, N. (1998). Binocular rivalry and visual awareness in human extrastriate cortex. Neuron 21, 753-759. doi: 10.1016/S0896-6273(00)80592-9
63. Tovee, M. J., Rolls, E. T., Treves, A., and Bellis, R. P. (1993). Information encoding and the responses of single neurons in the primate temporal visual cortex. J. Neurophysiol. 70, 640-654.
64. Tsao, D. Y., Freiwald, W. A., Tootell, R. B., and Livingstone, M. S. (2006). A cortical region consisting entirely of face-selective cells. Science 311, 670-674. doi: 10.1126/science.1119983
65. Wang, R., Li, J., Fang, H., Tian, M., and Liu, J. (2012). Individual differences in holistic processing predict face recognition ability. Psychol. Sci. 23, 169-177. doi: 10.1177/0956797611420575
66. Weigelt, S., Koldewyn, K., Dilks, D. D., Balas, B., McKone, E., and Kanwisher, N. (2014). Domain-specific development of face memory but not face perception. Dev. Sci. 17, 47-58. doi: 10.1111/desc.12089
67. Weiner, K. S., and Grill-Spector, K. (2010). Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage 52, 1559-1573. doi: 10.1016/j.neuroimage.2010.04.262
68. Wilhelm, O., Herzmann, G., Kunina, O., Danthiir, V., Schacht, A., and Sommer, W. (2010). Individual differences in perceiving and recognizing faces-One element of social cognition. J. Pers. Soc. Psychol. 99, 530-548. doi: 10.1037/a0019972
69. 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. doi: 10.1152/jn.00155.2004
70. Wojciulik, E., Kanwisher, N., and Driver, J. (1998). Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. J. Neurophysiol. 79, 1574-1578.
71. Yarkoni, T. (2009). Big correlations in little studies: Inflated fMRI correlations reflect low statistical power-Commentary on Vul et al. (2009). Perspect. Psychol. Sci. 4, 294-298. doi: 10.1111/j.1745-6924.2009.01127.x
72. Yin, R. K. (1969). Looking at upside-down faces. J. Exp. Psychol. 81, 141-145. doi: 10.1037/h0027474
73. Yovel, G., and Kanwisher, N. (2005). The neural basis of the behavioral face-inversion effect. Curr. Biol. 15, 2256-2262. doi: 10.1016/j.cub.2005.10.072
74. Zhang, J., Li, X., Song, Y., and Liu, J. (2012). The fusiform face area is engaged in holistic, not parts-based, representation of faces. PLoS ONE 7:e40390. doi: 10.1371/journal.pone.0040390
75. Zhu, Q., Zhang, J., Luo, Y. L., Dilks, D. D., and Liu, J. (2011). Resting-state neural activity across face-selective cortical regions is behaviorally relevant. J. Neurosci. 31, 10323-10330. doi: 10.1523/JNEUROSCI.0873-11.2011