Neural basis of identity information extraction from noisy face images

Journal of Neuroscience

Volumn 35, Issue 18, 2015, Pages 7165-7173

  Hermann, Petra ^a,b   Bankó, Éva M ^a   Gál, Viktor ^a,c   Vidnyánszky, Zoltán ^a,d  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d BUDAPEST UNIVERSITY OF TECHNOLOGY AND ECONOMICS   (Hungary)

Author keywords

Fusiform face area; Lateral occipital cortex; Resting state fMRI

Indexed keywords

ARTICLE; BEHAVIOR; BRAIN FUNCTION; CONNECTOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM FACE AREA; FUSIFORM GYRUS; HUMAN; IDENTITY; IMAGE PROCESSING; MALE; NEUROMODULATION; NORMAL HUMAN; OCCIPITAL CORTEX; PERCEPTION; PRIORITY JOURNAL; PSYCHOPHYSICS; RESTING STATE NETWORK; STIMULUS; TASK PERFORMANCE; VISION; VISUAL DISCRIMINATION LEARNING TEST; ADULT; BRAIN MAPPING; CONTROLLED STUDY; FACIAL EXPRESSION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PERCEPTIVE DISCRIMINATION; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; VISUAL CORTEX; YOUNG ADULT;

ADULT; BRAIN MAPPING; DISCRIMINATION (PSYCHOLOGY); FACIAL EXPRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84929377028     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3572-14.2015     Document Type: Article

References (87)

1. Baird LM, Burton AM (2008) The bilateral advantage for famous faces: in-terhemispheric communication or competition? Neuropsychologia 46: 1581-1587. CrossRef Medline
2. Bankó EM, Gál V, Körtvélyes J, Kovács G, Vidnyánszky Z (2011) Dissociating the effect of noise on sensory processing and overall decision difficulty. J Neurosci 31:2663-2674. CrossRef Medline
3. Bankó ÉM, Körtvélyes J, Weiss B, Vidnyánszky Z (2013) How the visual cortex handles stimulus noise: insights from amblyopia. PLoS One 8:e66583. CrossRef Medline
4. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541. CrossRef Medline
5. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10:433-436. CrossRef Medline
6. Cauchoix M, Barragan-Jason G, Serre T, Barbeau EJ (2014) The neural dynamics of face detection in the wild revealed by MVP A. J Neurosci 34: 846-854. CrossRef Medline
7. Clark VP, Parasuraman R, Keil K, Kulansky R, Fannon S, Maisog JM, Ungerleider LG, Haxby JV (1997) Selective attention to face identity and color studied with fMRI. Hum Brain Mapp 5:293-297. CrossRef Medline
8. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. Am J Neuroradiol 22:1326-1333. Medline
9. Crouzet SM, Kirchner H, Thorpe SJ (2010) Fast saccades toward faces: face detection in just 100 ms. J Vis 10(4):16.1-17. CrossRef Medline
10. 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. CrossRef Medline
11. Davies-Thompson J, Andrews TJ (2012) Intra-and interhemispheric connectivity between face-selective regions in the human brain. J Neurophysiol 108:3087-3095. CrossRef Medline
12. DiCarlo JJ, Cox DD (2007) Untangling invariant object recognition. Trends Cogn Sci 11:333-341. CrossRef Medline
13. Epstein RA, Higgins JS, Parker W, Aguirre GK, Cooperman S (2006) Cortical correlates of face and scene inversion: a comparison. Neuropsychologia 44:1145-1158. CrossRef Medline
14. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711. CrossRef Medline
15. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673-9678. CrossRef Medline
16. Furl N, Garrido L, Dolan RJ, Driver J, Duchaine B (2011) Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. J Cogn Neurosci 23:1723-1740. CrossRef Medline
17. Geusebroek J-M, Burghouts GJ, Smeulders AWM (2005) The Amsterdam Library of Object Images. Int J Comput Vis 61:103-112. CrossRef
18. Gilaie-Dotan S, Gelbard-Sagiv H, Malach R (2010) Perceptual shape sensitivity to upright and inverted faces is reflected in neuronal adaptation. Neuroimage 50:383-395. CrossRef Medline
19. Goffaux V, Peters J, Haubrechts J, Schiltz C, Jansma B, Goebel R (2011) From coarse to fine? Spatial and temporal dynamics of cortical face processing. Cereb Cortex 21:467-476. CrossRef Medline
20. Grill-Spector K, Weiner KS (2014) The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 15: 536-548. CrossRef Medline
21. 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. CrossRef Medline
22. Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41:1409-1422. CrossRef Medline
23. Grill-Spector K, Knouf N, Kanwisher N (2004) The fusiform face area subserves face perception, not generic within-category identification. Nat Neurosci 7:555-562. CrossRef Medline
24. Harris A, Aguirre GK (2010) Neural tuning for face wholes and parts in human fusiform gyrus revealed by fMRI adaptation. J Neurophysiol 104: 336-345. CrossRef Medline
25. Hasson U, Harel M, Levy I, Malach R (2003) Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37:1027-1041. CrossRef Medline
26. Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223-233. CrossRef Medline
27. Heekeren HR, Marrett S, Bandettini PA, Ungerleider LG (2004) A general mechanism for perceptual decision-making in the human brain. Nature 431:859-862. CrossRef Medline
28. Hegdé J (2008) Time course of visual perception: coarse-to-fine processing and beyond. Prog Neurobiol 84:405-439. CrossRef Medline
29. Hochstein S, Ahissar M (2002) View from the top: hierarchies and reverse hierarchies in the visual system. Neuron 36:791-804. CrossRef Medline
30. Horovitz SG, Rossion B, Skudlarski P, Gore JC (2004) Parametric design and correlational analyses help integrating fMRI and electrophysiological data during face processing. Neuroimage 22:1587-1595. CrossRef Medline
31. Huang L, Song Y, Li J, Zhen Z, Yang Z, Liu J (2014) Individual differences in cortical face selectivity predict behavioral performance in face recognition. Front Hum Neurosci 8:483. CrossRef Medline
32. Jiang F, Dricot L, Weber J, Righi G, Tarr MJ, Goebel R, Rossion B (2011) Face categorization in visual scenes may start in a higher order area of the right fusiform gyrus: evidence from dynamic visual stimulation in neuro-imaging. J Neurophysiol 106:2720-2736. CrossRef Medline
33. 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. Medline
34. Kayser AS, Erickson DT, Buchsbaum BR, D'Esposito M (2010) Neural representations of relevant and irrelevant features in perceptual decision making. J Neurosci 30:15778-15789. CrossRef Medline
35. Larsson J, Heeger DJ (2006) Two retinotopic visual areas in human lateral occipital cortex. J Neurosci 26:13128-13142. CrossRef Medline
36. 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. CrossRef Medline
37. Lewis MB, Edmonds AJ (2003) Face detection: mapping human performance. Perception 32:903-920. CrossRef Medline
38. Liu J, Harris A, Kanwisher N (2002) Stages of processing in face perception: an MEG study. Nat Neurosci 5:910-916. CrossRef Medline
39. Lobmaier JS, Klaver P, Loenneker T, Martin E, Mast FW (2008) Featural and confìgural face processing strategies: evidence from a functional magnetic resonance imaging study: Neuroreport 19:287-291. CrossRef
40. 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 U S A 92:8135-8139. CrossRef Medline
41. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, et al. (2001a) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293-1322. CrossRef Medline
42. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, et al. (2001b) A four-dimensional probabilistic atlas of the human brain. J Am Med Inform Assoc 8:401-430. CrossRef Medline
43. Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J (1995) A probabilistic atlas of the human brain: theory and rationale for its development. The International Consortium for Brain Mapping (ICBM). Neuroimage 2:89-101. CrossRef Medline
44. McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9:605-610. CrossRef Medline
45. Meng M, Cherian T, Singal G, Sinha P (2012) Lateralization of face processing in the human brain. Proc Biol Sci 279:2052-2061. CrossRef Medline
46. Minnebusch DA, Suchan B, Köster O, Daum I (2009) A bilateral occipitotemporal network mediates face perception. Behav Brain Res 198:179-185. CrossRef Medline
47. Mohr B, Landgrebe A, Schweinberger SR (2002) Interhemispheric cooperation for familiar but not unfamiliar face processing. Neuropsychologia 40:1841-1848. CrossRef Medline
48. O'Craven KM, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Nature 401:584-587. CrossRef Medline
49. O'Neil EB, Hutchison RM, McLean DA, Köhler S (2014) Resting-state fMRI reveals functional connectivity between face-selective perirhinal cortex and the fusiform face area related to face inversion. Neuroimage 92:349-355. CrossRef Medline
50. Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437-442. CrossRef Medline
51. Pernet CR, Wilcox R, Rousselet GA (2012) Robust correlation analyses: false positive and power validation using a new open source MATLAB toolbox. Front Psychol 3:606. CrossRef Medline
52. Pinsk MA, Arcaro M, Weiner KS, Kalkus JF, Inati SJ, Gross CG, Kastner S (2009) Neural representations of faces and body parts in macaque and human cortex: a comparative fMRI study. J Neurophysiol 101:2581-2600. CrossRef Medline
53. Pitcher D, Duchaine B, Walsh V, Kanwisher N (2010) TMS evidence for feedforward and feedback mechanisms of face and body perception. J Vis 10(7) :671. CrossRef
54. Pitcher D, Duchaine B, Walsh V, Yovel G, Kanwisher N (2011a) The role of lateral occipital face and object areas in the face inversion effect. Neuropsychologia 49:3448-3453. CrossRef Medline
55. Pitcher D, Walsh V, Duchaine B (2011b) The role of the occipital face area in the cortical face perception network. Exp Brain Res 209:481-493. CrossRef Medline
56. Rainer G, Augath M, Trinath T, Logothetis NK (2001) Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey. Curr Biol 11:846-854. CrossRef Medline
57. Rainer G, Augath M, Trinath T, Logothetis NK (2002) The effect of image scrambling on visual cortical BOLD activity in the anesthetized monkey. Neuroimage 16:607-616. CrossRef Medline
58. Reddy L, Moradi F, Koch C (2007) Top-down biases win against focal attention in the fusiform face area. Neuroimage 38:730-739. CrossRef Medline
59. Reinholz J, Pollmann S (2007) Neural basis of redundancy effects in visual object categorization. Neurosci Lett 412:123-128. CrossRef Medline
60. Righart R, Andersson F, Schwartz S, Mayer E, Vuilleumier P (2010) Top-down activation of fusiform cortex without seeing faces in prosopagnosia. Cereb Cortex 20:1878-1890. CrossRef Medline
61. Rossion B (2008) Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. Neuroimage 40:423-426. CrossRef Medline
62. Rossion B, Dricot L, Devolder A, Bodart JM, Crommelinck M, De Gelder B, Zoontjes R (2000) Hemispheric asymmetries for whole-based and part-based face processing in the human fusiform gyrus. J Cogn Neurosci 12:793-802. CrossRef Medline
63. 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. CrossRef Medline
64. Rossion B, Hanseeuw B, Dricot L (2012) Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis. Brain Cogn 79:138-157. CrossRef Medline
65. Rotshtein P, Geng JJ, Driver J, Dolan RJ (2007a) Role of features and second-order spatial-relations in face discrimination, face recognition, and individual face skills. J Cogn Neurosci 19:1435-1452. CrossRef Medline
66. Rotshtein P, Vuilleumier P, Winston J, Driver J, Dolan R (2007b) Distinct and convergent visual processing of high and low spatial frequency information in faces. Cereb Cortex 17:2713-2724. CrossRef Medline
67. Rousselet GA, Macé MJ, Fabre-Thorpe M (2003) Is it an animal? Is it a human face? Fast processing in upright and inverted natural scenes. J Vis 3(6):440-455. CrossRef Medline
68. Schweinberger SR, Baird LM, Blümler M, Kaufmann JM, Mohr B (2003) Interhemispheric cooperation for face recognition but not for affective facial expressions. Neuropsychologia 41:407-414. CrossRef Medline
69. Silson EH, McKeefry DJ, Rodgers J, Gouws AD, Hymers M, Morland AB (2013) Specialized and independent processing of orientation and shape in visual field maps LOl and L02. Nat Neurosci 16:267-269. CrossRef Medline
70. Steeves J, Dricot L, Goltz HC, Sorger B, Peters J, Milner AD, Goodale MA, Goebel R, Rossion B (2009) Abnormal face identity coding in the middle fusiform gyrus of two brain damaged prosopagnosic patients. Neuropsychologia 47:2584-2592. CrossRef Medline
71. Tang H, Buia C, Madhavan R, Crone NE, Madsen JR, Anderson WS, Kreiman G (2014) Spatiotemporal dynamics underlying object completion in human ventral visual cortex. Neuron 83:736-748. CrossRef Medline
72. Tiddeman B, Burt M, Perrett D (2001) Prototyping and transforming facial textures for perception research. IEEE Comput Graph Appl 21:42-50. CrossRef
73. Tjan BS, Lestou V, Kourtzi Z (2006) Uncertainty and Invariance in the Human Visual Cortex. J Neurophysiol 96:1556-1568. CrossRef Medline
74. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Del-croix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289. CrossRef Medline
75. Wang X, Han Z, He Y, Caramazza A, Song L, Bi Y (2013) Where color rests: spontaneous brain activity of bilateral fusiform and lingual regions predicts object color knowledge performance. Neuroimage 76:252-263. CrossRef Medline
76. Weiner KS, Grill-Spector K (2010) Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage 52: 1559-1573. CrossRef Medline
77. Weiner KS, Sayres R, Vinberg J, Grill-Spector K (2010) fMRI-adaptation and category selectivity in human ventral temporal cortex: regional differences across time scales. J Neurophysiol 103:3349-3365. CrossRef Medline
78. Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windisch-berger C (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies. Neuroimage 47:1408-1416. CrossRef Medline
79. Wojciulik E, Kanwisher N, Driver J (1998) Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. J Neurophysiol 79:1574-1578. Medline
80. Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8:e68910. CrossRef Medline
81. Yovel G, Kanwisher N (2004) Face perception: domain specific, not process specific. Neuron 44:889-898. CrossRef Medline
82. Yovel G, Kanwisher N (2005) The neural basis of the behavioral face-inversion effect. Curr Biol 15:2256-2262. CrossRef Medline
83. Yovel G, Tambini A, Brandman T (2008) The asymmetry of the fusiform face area is a stable individual characteristic that underlies the left-visual-field superiority for faces. Neuropsychologia 46:3061-3068. CrossRef Medline
84. Zhang H, Tian J, Liu J, Li J, Lee K (2009) Intrinsically organized network for face perception during the resting state. Neurosci Lett 454:1-5. CrossRef Medline
85. Zhang J, Li X, Song Y, Liu J (2012) The fusiform face area is engaged in holistic, not parts-based, representation of faces. PLoS One 7:e40390. CrossRef Medline
86. Zhen Z, Fang H, Liu J (2013) The hierarchical brain network for face recognition. PLoS One 8:e59886. CrossRef Medline
87. Zhu Q, Zhang J, Luo YL, Dilks DD, Liu J (2011) Resting-state neural activity across face-selective cortical regions is behaviorally relevant. J Neurosci 31:10323-10330. CrossRef Medline