Dissociation of part-based and integrated neural responses to faces by means of electroencephalographic frequency tagging

European Journal of Neuroscience

Volumn 40, Issue 6, 2014, Pages 2987-2997

  Boremanse, Adriano ^a   Norcia, Anthony M ^b   Rossion, Bruno ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Face perception; Frequency tagging; Human; Intermodulation; Repetition suppression; Steady state visual evoked potential

Indexed keywords

ADULT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; ELECTROENCEPHALOGRAPHIC FREQUENCY TAGGING; ELECTROENCEPHALOGRAPHY; EVOKED VISUAL RESPONSE; FACIES; FEMALE; FUNCTIONAL DISSOCIATION; HUMAN; HUMAN EXPERIMENT; MALE; NERVE POTENTIAL; NORMAL HUMAN; OCCIPITAL CORTEX; PATTERN RECOGNITION; PRIORITY JOURNAL; TEMPORAL CORTEX; VISUAL DISCRIMINATION; VISUAL STIMULATION; BRAIN; FACE; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; SIGNAL PROCESSING; YOUNG ADULT;

ADULT; BRAIN; ELECTROENCEPHALOGRAPHY; FACE; FEMALE; HUMANS; MALE; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; SIGNAL PROCESSING, COMPUTER-ASSISTED; YOUNG ADULT;

EID: 84908328250     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12663     Document Type: Article

References (71)

1. Ahumada, A.J. Jr. & Lovell, J. (1971) Stimulus features in signal detection. J. Acoust. Soc. Am., 49, 1751-1756.
2. Aissani, C., Cottereau, B., Dumas, G., Paradis, A.L. & Lorenceau, J. (2011) Magnetoencephalographic signatures of visual form and motion binding. Brain Res., 1408, 27-40.
3. Alonso-Prieto, E., Belle, G.V., Liu-Shuang, J., Norcia, A.M. & Rossion, B. (2013) The 6 Hz fundamental stimulation frequency rate for individual face discrimination in the right occipito-temporal cortex. Neuropsychologia, 51, 2863-2875.
4. Andersen, S.K., Müller, M.M. & Hillyard, S.A. (2009) Color-selective attention need not be mediated by spatial attention. J. Vision, 9, 1-7.
5. Andrews, T.J., Davies-Thompson, J., Kingstone, A. & Young, A.W. (2010) Internal and external features of the face are represented holistically in face-selective regions of visual cortex. J. Neurosci., 30, 3544-3552.
6. Appelbaum, L.G., Wade, A.R., Vildavski, V.Y., Pettet, M.W. & Norcia, A.M. (2006) Cue-invariant networks for figure and background processing in human visual cortex. J. Neurosci., 26, 11695-11708.
7. Appelbaum, L., Wade, A., Pettet, M.W., Vildavski, V.Y. & Norcia, A.M. (2008) Figure-ground interaction in the human visual cortex. J. Vision, 8, 1-19.
8. Axelrod, V. & Yovel, G. (2010) External facial features modify the representation of internal facial features in the fusiform face area. NeuroImage, 52, 720-725.
9. Bentin, S., McCarthy, G., Perez, E., Allison, T. & Puce, A. (1996) Electrophysiological studies of face perception in humans. J. Cognitive Neurosci., 8, 551-565.
10. Biederman, I. (1987) Recognition-by-components: a theory of human image understanding. Psychol. Rev., 94, 115-147.
11. Biederman, I. & Kalocsai, P. (1997) Neurocomputational bases of object and face recognition. Philos. T. Roy. Soc. B., 352, 1203-1219.
12. Boremanse, A., Norcia, A.M. & Rossion, B. (2013) An objective neural signature for visual binding of face parts in the human brain. J. Vision, 13, 1-18.
13. Bullier, J. (2001) Integrated model of visual processing. Brain Res. Rev., 36, 96-107.
14. DeGutis, J., Wilmer, J., Mercado, R.J. & Cohan, S. (2013) Using regression to measure holistic face processing reveals a strong link with face recognition ability. Cognition, 126, 87-100.
15. Di Russo, F. & Spinelli, D. (2002) Effects of sustained, voluntary attention on amplitude and latency of steady-state visual evoked potential: a costs and benefits analysis. Clin. Neurophysiol., 113, 1771-1777.
16. DiCarlo, J.J. & Cox, D.D. (2007) Untangling invariant object recognition. Trends Cogn. Sci., 11, 333-341.
17. Fuchs, S., Andersen, S.K., Gruber, T. & Müller, M.M. (2008) Attentional bias of competitive interactions in neuronal networks of early visual processing in the human brain. NeuroImage, 41, 1086-1101.
18. Giani, A.S., Ortiz, E., Belardinelli, P., Kleiner, M., Preissl, H. & Noppeney, U. (2012) Steady-state responses in MEG demonstrate information integration within but not across the auditory and visual senses. NeuroImage, 60, 1478-1489.
19. Grill-Spector, K., Henson, R. & Martin, A. (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci., 10, 14-23.
20. Haig, N.D. (1985) How faces differ - a new comparative technique. Perception, 14, 601-615.
21. Harris, A. & Aguirre, G.K. (2010) Neural tuning for face wholes and parts in human fusiform gyrus revealed by FMRI adaptation. J. Neurophysiol., 104, 336-345.
22. Hochstein, S. & Ahissar, M. (2002) View from the top: hierarchies and reverse hierarchies review. Neuron, 36, 791-804.
23. Hole, G.J. (1994) Configurational factors in the perception of unfamiliar faces. Perception, 23, 65-74.
24. Hou, C., Good, W.V. & Norcia, A.M. (2007) Validation study of VEP vernier acuity in normal-vision and amblyopic adults. Invest. Ophth. Vis. Sci., 48, 4070-4078.
25. Hsiao, J.H. & Cottrell, G. (2008) Two fixations suffice in face recognition. Psychol. Sci., 19, 998-1006.
26. Jacques, C. & Rossion, B. (2009) The initial representation of individual faces in the right occipito-temporal cortex is holistic: electrophysiological evidence from the composite face illusion. J. Vision, 9, 1-16.
27. Jiang, X., Rosen, E., Zeffiro, 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.
28. 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.
29. Klimesch, W. (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Rev., 29, 169-195.
30. Lai, J., Pancaroglu, R., Oruc, I., Barton, J.J. & Davies-Thompson, J. (2014) Neuroanatomic correlates of the feature-salience hierarchy in face processing: an fMRI-adaptation study. Neuropsychologia, 53, 274-283.
31. Logothetis, N.K. & Sheinberg, D.L. (1996) Visual object recognition. Annu. Rev. Neurosci., 19, 577-621.
32. Marr, D. (1982) Vision: A Computational Investigation into the Human Representation and Processing of Visual Information, Phenomenology and the Cognitive Sciences. Freeman, New York.
33. Maurer, D., Grand, R.L. & Mondloch, C.J. (2002) The many faces of configural processing. Trends Cogn. Sci., 6, 255-260.
34. McTeague, L.M., Shumen, J.R., Wieser, M.J., Lang, P.J. & Keil, A. (2011) Social vision: sustained perceptual enhancement of affective facial cues in social anxiety. NeuroImage, 54, 1615-1624.
35. Miller, E., Li, L. & Desimone, R. (1991) A neural mechanism for working and recognition memory in inferior temporal cortex. Science, 254, 1377-1379.
36. Mouraux, A. & Iannetti, G.D. (2008) Across-trial averaging of event-related EEG responses and beyond. Magn. Reson. Imaging, 26, 1041-1054.
37. Müller, M.M., Teder-Sälejärvi, W. & Hillyard, S.A. (1998) The time course of cortical facilitation during cued shifts of spatial attention. Nat. Neurosci., 1, 631-634.
38. Müller, M.M., Andersen, S., Trujillo, N.J., Valdés-Sosa, P., Malinowski, P. & Hillyard, S.A. (2006) Feature-selective attention enhances color signals in early visual areas of the human brain. Proc. Natl. Acad. Sci. USA, 103, 14250-14254.
39. Mumford, D. (1992) On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Cybernetics, 251, 241-251.
40. Norcia, A.M., Wesemann, W. & Manny, R.E. (1999) Electrophysiological correlates of vernier and relative motion mechanisms in human visual cortex. Visual Neurosci., 16, 1123-1131.
41. Peterson, M.F. & Eckstein, M.P. (2012) Looking just below the eyes is optimal across face recognition tasks. Proc. Natl. Acad. Sci. USA, 109, E3314-E3323.
42. Purcell, D. & Stewart, A. (1988) The face-detection effect: configuration enhances detection. Percept. Psychophys., 43, 355-366.
43. Ratliff, F. & Zemon, V. (1982) Some new methods for the analysis of lateral interactions that influence the visual evoked potential. Ann. NY Acad. Sci., 388, 113-124.
44. Regan, D. (1966) Some characteristics of average steady-state and transient responses evoked by modulated light. Electroen. Clin. Neuro., 20, 238-248.
45. Regan, D. (1989) Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine. Elsevier, New York.
46. Regan, D. & Heron, J.R. (1969) Clinical investigation of lesions of the visual pathway: a new objective technique. J. Neurol. Neurosur. Ps., 32, 479-483.
47. Regan, M.P. & Regan, D. (1988) A frequency domain technique for characterizing nonlinearities in biological systems. J. Theor. Biol., 133, 293-317.
48. Ringo, J. (1996) Stimulus specific adaptation in inferior temporal and medial temporal cortex of the monkey. Behav. Brain Res., 76, 101-107.
49. Rossion, B. (2008a) Picture-plane inversion leads to qualitative changes of face perception. Acta Psychol., 128, 274-289.
50. Rossion, B. (2008b) Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. NeuroImage, 40, 423-426.
51. Rossion, B. (2013) The composite face illusion: a whole window into our understanding of holistic face perception. Vis. Cogn., 21, 139-253.
52. Rossion, B. (2014) Understanding individual face discrimination by means of fast periodic visual stimulation. Exp. Brain Res., 232, 1599-1621.
53. Rossion, B. & Boremanse, A. (2011) Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. J. Vision, 11, 1-21.
54. Rossion, B., Dricot, L., Goebel, R. & Busigny, T. (2011) Holistic face categorization in higher order visual areas of the normal and prosopagnosic brain: toward a non-hierarchical view of face perception. Front. Hum. Neurosci., 4, 225.
55. Rossion, B., Prieto, E.A., Boremanse, A., Kuefner, D. & Van Belle, G. (2012) A steady-state visual evoked potential approach to individual face perception: effect of inversion, contrast-reversal and temporal dynamics. NeuroImage, 63, 1585-1600.
56. Schiltz, C. & Rossion, B. (2006) Faces are represented holistically in the human occipito-temporal cortex. NeuroImage, 32, 1385-1394.
57. Schiltz, C., Dricot, L., Goebel, R. & Rossion, B. (2010) Holistic perception of individual faces in the right middle fusiform gyrus as evidenced by the composite face illusion. J. Vision, 10, 1-16.
58. Schyns, P.G., Petro, L.S. & Smith, M.L. (2007) Dynamics of visual information integration in the brain for categorizing facial expressions. Curr. Biol., 17, 1580-1585.
59. Sergent, J. (1984) An investigation into component and configural processes underlying face perception. Brit. J. Psychol., 75, 225-242.
60. Smith, M.L., Fries, P., Gosselin, F., Goebel, R. & Schyns, P.G. (2009) Inverse mapping the neuronal substrates of face categorizations. Cereb. Cortex, 19, 2428-2438.
61. Srinivasan, R., Bibi, F.A. & Nunez, P.L. (2006) Steady-state visual evoked potentials: distributed local sources and wave-like dynamics are sensitive to flicker frequency. Brain Topogr., 18, 167-187.
62. Sutoyo, D. & Srinivasan, R. (2009) Nonlinear SSVEP responses are sensitive to the perceptual binding of visual hemifields during conventional "eye" rivalry and interocular "percept" rivalry. Brain Res., 1251, 245-255.
63. Tanaka, J. & Farah, M. (1993) Parts and wholes in face recognition. Q. J. Exp. Psychol., 46, 225-245.
64. Thorpe, S., Fize, D. & Marlot, C. (1996) Speed of processing in the human visual system. Nature, 381, 520-522.
65. Tsai, J., Wade, A. & Norcia, A. (2012) Dynamics of normalization underlying masking in human visual cortex. J. Neurosci., 32, 2783-2789.
66. Ullman, S. (2007) Object recognition and segmentation by a fragment-based hierarchy. Trends Cogn. Sci., 11, 58-64.
67. Victor, J.D. & Conte, M.M. (2000) Two-frequency analysis of interactions elicited by Vernier stimuli. Visual Neurosci., 17, 959-973.
68. Yin, R. (1969) Looking at upside-down faces. J. Exp. Psychol., 81, 141-151.
69. Young, A., Hellawell, D. & Hay, D. (1987) Configurational information in face perception. Perception, 16, 747-759.
70. Zemon, V. & Ratliff, F. (1982) Visual evoked potentials: evidence for lateral interactions. Proc. Natl. Acad. Sci. USA, 79, 5723-5726.
71. Zemon, V. & Ratliff, F. (1984) Intermodulation components of the visual evoked potential: responses to lateral and superimposed stimuli. Biol. Cybern., 50, 401-408.