[en] Discrimination of facial identities is a fundamental function of the human brain that is challenging to examine with macroscopic measurements of neural activity, such as those obtained with functional magnetic resonance imaging (fMRI) and electroencephalography (EEG). Although visual adaptation or repetition suppression (RS) stimulation paradigms have been successfully implemented to this end with such recording techniques, objective evidence of an identity-specific discrimination response due to adaptation at the level of the visual representation is lacking. Here, we addressed this issue with fast periodic visual stimulation (FPVS) and EEG recording combined with a symmetry/asymmetry adaptation paradigm. Adaptation to one facial identity is induced through repeated presentation of that identity at a rate of 6 images per second (6 Hz) over 10 sec. Subsequently, this identity is presented in alternation with another facial identity (i.e., its anti-face, both faces being equidistant from an average face), producing an identity repetition rate of 3 Hz over a 20 sec testing sequence. A clear EEG response at 3 Hz is observed over the right occipito-temporal (ROT) cortex, indexing discrimination between the two facial identities in the absence of an explicit behavioral discrimination measure. This face identity discrimination occurs immediately after adaptation and disappears rapidly within 20 sec. Importantly, this 3 Hz response is not observed in a control condition without the single-identity 10 sec adaptation period. These results indicate that visual adaptation to a given facial identity produces an objective (i.e., at a pre-defined stimulation frequency) electrophysiological index of visual discrimination between that identity and another, and provides a unique behavior-free quantification of the effect of visual adaptation.
Disciplines :
Neurosciences & behavior
Author, co-author :
RETTER, Talia ; Psychological Sciences Research Institute, Institute of Neuroscience, University of Louvain, Louvain-la-Neuve, Belgium. Electronic address: talia.retter@uclouvain.be
Rossion, Bruno; Psychological Sciences Research Institute, Institute of Neuroscience, University of Louvain, Louvain-la-Neuve, Belgium. Electronic address: bruno.rossion@uclouvain.be
External co-authors :
yes
Language :
English
Title :
Visual adaptation provides objective electrophysiological evidence of facial identity discrimination.
Publication date :
July 2016
Journal title :
Cortex: A Journal Devoted to the Study of the Nervous System and Behavior
Belgian National Fund for Scientific Research European Research Council
Funding text :
TR is supported by the Belgian National Fund for Scientific Research (Fonds de la Recherche Scientifique; FNRS: FC7159 ). This work was also supported by a grant from the European Research Council (ERC: facessvep 284025 ) to BR. We would like to thank Renaud Laguesse for preparing the original face photographs and Milena Dzhelyova for her help with creating the face/anti-face stimulus pairs.
Ales, J.M., Farzin, F., Rossion, B., Norcia, A.M., An objective method for measuring face detection thresholds using the sweep steady-state visual evoked response. Journal of Vision 12:10 (2012), 1–18.
Ales, J.M., Norcia, A.M., Assessing direction-specific adaptation using the steady-state visual evoked potential: results from EEG source imaging. Journal of Vision 9:7 (2009), 1–13.
Alonso-Prieto, E.A., Van Belle, G., Liu-Shuang, J., Norcia, A.M., Rossion, B., The 6Hz fundamental frequency rate for individual face discrimination in the right occipito-temporal cortex. Neuropsychologia 51 (2013), 2863–2975.
Amihai, I., Deouell, L.Y., Bentin, S., Neural adaptation is related to face repetition irrespective of identity: a reappraisal of the N170 effect. Experimental Brain Research 209:2 (2012), 193–204.
Andrews, T.J., Davies-Thompson, J., Kingstone, A., Young, A.W., Internal and external features of the face are represented holistically in face-selective regions of visual cortex. Journal of Neuroscience 30:9 (2010), 3544–3552.
Andrews, T.J., Ewbank, M.P., Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. NeuroImage 23 (2004), 905–913.
Appelbaum, L.G., Norcia, A.M., Attentive and pre-attentive aspects of figural processing. Journal of Vision 9:11 (2009), 1–12.
Balas, B., Cox, D., Conwell, E., The effect of real-world personal familiarity on the speed of face information processing. PLoS One, 2(11), 2007, e1223.
Bentin, S., McCarthy, G., Perez, E., Puce, A., Allison, T., Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience 8 (1996), 551–565.
Benton, A.L., Van Allen, M.W., Prosopagnosia and facial discrimination. Journal of the Neurological Sciences 15 (1968), 167–172.
Bindemann, M., Burton, A.M., Leuthold, H., Schweinberger, S.R., Brain potential correlates of face recognition: geometric distortions and the N250r brain response to stimulus repetitions. Psychphysiology 45:4 (2008), 535–544.
Busigny, T., Rossion, B., Acquired prosopagnosia abolishes the face inversion effect. Cortex 46 (2010), 965–981 Read more: http://face-categorization-lab.webnode.com/publications/.
Caharel, S., d'Arripe, O., Ramon, M., Jacques, C., Rossion, B., Early adaptation to unfamiliar faces across viewpoint changes in the right hemisphere: evidence from the N170 ERP component. Neuropsychologia 47 (2009), 639–643.
Caharel, S., Collet, K., Rossion, B., The early visual encoding of a face (N170) is viewpoint-dependent: a parametric ERP-adaptation study. Biological Psychology 106 (2015), 18–27.
Caharel, S., Jacques, C., d'Arripe, O., Ramon, M., Rossion, B., Early electrophysiological correlates of adaptation to personally familiar and unfamiliar faces across viewpoint changes. Brain Research 1387 (2011), 85–98.
Caharel, S., Jiang, F., Blanz, V., Rossion, B., Recognizing an individual face: 3D shape contributes earlier than 2D surface reflectance information. NeuroImage 47 (2009), 1809–1818.
Carbon, C.C., Famous faces as icons. The illusion of being an expert in the recognition of famous faces. Perception 2008:37 (2008), 801–806.
Cottereau, B.R., McKee, S.P., Ales, J.M., Norcia, A.M., Disparity-tuned population responses from human visual cortex. Journal of Neuroscience 31:3 (2011), 954–965.
Davidesco, I., Zion-Golumbic, E., Bickel, S., Harel, M., Groppe, D.M., Keller, C.J., et al. Exemplar selectivity reflects perceptual similarities in the human fusiform cortex. Cerebral Cortex 24 (2014), 1879–1893.
Davies-Thompson, J., Gouws, A., Andrews, T.J., An image-dependent representation of familiar and unfamiliar faces in the human ventral stream. Neuropsychologia 47 (2009), 1627–1635.
Dubois, J., de Berker, A.O., Tsao, D.Y., Single-unit recordings in the macaque face patch system reveal limitations of fMRI MVPA. Journal of Neuroscience 35:6 (2015), 2791–2802.
Dzhelyova, M., Rossion, B., The effect of parametric stimulus size variation on individual face discrimination indexed by fast periodic visual stimulation. BMC Neuroscience 15:87 (2014), 1–12.
Engell, A.D., McCarthy, G., Repetition suppression of face-selective evoked and induced EEG recorded from human cortex. Human Brain Mapping 35 (2014), 4155–4162.
Ewbank, M.P., Andrews, T.J., Differential sensitivity for viewpoint between familiar and unfamiliar faces in human visual cortex. NeuroImage 40 (2008), 1857–1870.
Ewbank, M.P., Henson, R.N., Rowe, J.B., Stoyanova, R.S., Calder, A.J., Different neural mechanisms within occipitotemporal cortex underlie repetition suppression across same and different-size faces. Cerebral Cortex 23 (2013), 1073–1084.
Faerber, S.J., Jürgen, M.K., Schweinberger, S.R., Early temporal negativity is sensitive to perceived (rather than physical) facial identity. Neurospcyologia 75 (2015), 132–142.
Freiwald, W.A., Tsao, D.Y., Livingstone, M.S., A face feature space in the macaque temporal lobe. Nature Neuroscience 12:9 (2009), 1187–1196.
Gauthier, I., Tarr, M.J., Moylan, J., Skudlarski, P., Gore, J.C., Anderson, A.W., The fusiform “face area” is part of a network that processes faces at the individual level. Journal of Cognitive Neuroscience 12:3 (2000), 495–504.
Gentile, F., Rossion, B., Temporal frequency tuning of cortical face-sensitive areas for individual face perception. NeuroImage 90 (2014), 256–265.
Goffaux, V., Schiltz, C., Mur, M., Goebel, R., Local discriminability determines the strength of holistic processing for faces in the fusiform face area. Frontiers in Psychology, 3, 2012, 604.
Gosaert, E., Op de Beeck, H.P., Representations of facial identity information in the ventral visual stream investigated with multivoxel pattern analyses. Journal of Neuroscience 33:19 (2013), 8549–8558.
Grill-Spector, K., Henson, R., Martin, A., Repetition and the brain: neural models of stimulus-specific effects. Trends in Cognitive Sciences 10:1 (2006), 14–23.
Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., Malach, R., Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24:1 (1999), 187–203.
Grill-Spector, K., Malach, R., fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychologica 107 (2001), 293–321.
Grotheer, M., Hermann, P., Vidnyánszky, Z., Kovács, G., Repetition probability effects for inverted faces. NeuroImage 102:2 (2014), 416–423.
Harris, R.J., Young, A.W., Andrew, T.J., Brain regions involved in processing facial identity and expression are differentially selective for surface and edge information. NeuroImage 97:100 (2014), 217–223.
Haxby, J.V., Hoffman, E.A., Gobbini, M.I., The distributed human neural system for face perception. Trends in Cognitive Science 4 (2000), 223–233.
Hecaen, H., Angelergues, R., Agnosia for faces (prosopagnosia). Archives of Neurology 7 (1962), 92–100.
de Heering, A., Rossion, B., Rapid categorization of natural face images in the infant right hemisphere. eLife, 4, 2015 e06564, 1–14.
Heinrich, S.P., Permutation-based significance tests for multiharmonic steady-state evoked potentials. IEEE Transactions on Biomedical Engineering 56:2 (2009), 534–537.
Heinrich, S.P., Some thoughts on the interpretation of steady-state evoked potentials. Documenta Ophthalmology 120 (2010), 205–214.
Heisz, J.J., Watter, S., Shedden, J.M., Automatic face identity encoding at the N170. Vision Research 46:28 (2006), 4604–4614.
Hillger, L.A., Koenig, O., Separable mechanisms in face processing: evidence from hemispheric specialization. Journal of Cognitive Neuroscience 3 (1991), 42–58.
Hsiao, J.H., Cottrell, G., Two fixations suffice in face recognition. Psychological Science 19 (2008), 998–1006.
Hyvarinen, A., Oja, E., Independent component analysis: algorithms and applications. Neural Networks 13 (2000), 411–430.
Itier, R.J., Taylor, M.J., Inversion and contrast polarity reversal affect both encoding and recognition processes of unfamiliar faces: a repetition study using ERPs. NeuroImage 15 (2002), 353–372.
Jacques, C., d'Arripe, O., Rossion, B., The time course of the inversion effect during individual face discrimination. Journal of Vision 7:8 (2007), 1–9.
Jacques, C., Rossion, B., The speed of individual face categorization. Psychological Science 17 (2006), 485–492.
Jenkins, R., White, D., Van Montfort, X., Burton, A.M., Variability in photos of the same face. Cognition 121:3 (2011), 313–323.
Jiang, F., Blanz, V., O'Toole, A.J., Probing the visual representation of faces with adaptation: a view from the other side of the mean. Psychological Science 17:6 (2006), 493–500.
Jiang, F., Dricot, L., Blanz, V., Goebel, R., Rossion, B., Neural correlates of shape and surface reflectance information in individual faces. Neuroscience 163 (2009), 1078–1091.
Knappmeyer, B., Thornton, I.M., Bülthoff, H.H., The use of facial motion and facial form during the processing of identity. Vision Research 43 (2003), 1921–1936.
Kovács, G., Zimmer, M., Harza, I., Vidnyánszky, Z., Adaptation duration affects the spatial selectivity of facial aftereffects. Vision Research 47:25 (2007), 3141–3149.
Kriegeskorte, N., Formisano, E., Sorger, B., Goebel, R., Individual faces elicit distinct response patterns in human anterior temporal cortex. Proceedings of the National Academy of Sciences 105:51 (2007), 20600–20605.
Leopold, D.A., Bondar, I.V., Giese, M.A., Norm-based face encoding by single neurons in monkey inferotemporal cortex. Nature 442 (2006), 572–575.
Leopold, D.A., Rhodes, G., Mueller, K., Jeffery, L., The dynamics of visual adaptation to faces. Philosophical Transactions of the Royal Society of London B 272 (2015), 897–904.
Liu-Shuang, J., Ales, J.M., Rossion, B., Norcia, A.M., The effect of contrast polarity reversal on face detection: evidence of perceptual asymmetry from sweep VEP. Vision Research 108 (2015), 8–19.
Liu-Shuang, J., Ales, J.M., Rossion, B., Norcia, A.M., Separable effects of inversion and contrast reversal on face detection thresholds and response functions: a sweep VEP study. Journal of Vision, 15(2), 2015.
Liu-Shuang, J., Norcia, A.M., Rossion, B., An objective index of individual face discrimination in the right occipito-temporal cortex by means of fast periodic visual stimulation. Neuropsychologia 52 (2014), 57–72.
Megreya, A.M., Burton, A.M., Unfamiliar faces are not faces: evidence from a matching task. Memory & Cognition 34 (2006), 865–876.
Meigen, T., Bach, M., On the statistical significance of electrophysiological steady-state responses. Documenta Ophthalmology 98 (1999), 207–232.
Meyers, E.M., Borzello, M., Freiwald, W.A., Tsao, D., Intelligent information loss: the coding of facial identity, head pose, and non-face information in the macaque face patch system. Journal of Neuroscience 35:18 (2015), 7069–7081.
Müller, M.M., Andersen, S., Trujillo, N.J., Valdes-Sosa, P., Malinowski, P., Hillyard, S.A., Feature-selective attention enhances color signals in early visual areas of the human brain. Proceedings of the National Academy of Sciences 103:38 (2006), 14250–14254.
Natu, V.S., Jiang, F., Narvekar, A., Keshvari, S., Blanz, V., O'Toole, A.J., Dissociable neural patterns of facial identity across changes in viewpoint. Journal of Cognitive Neuroscience 22:7 (2010), 1570–1582.
Nemrodov, D., Jacques, C., Rossion, B., The temporal dynamics of periodic electrophysiological responses to face-identity adaptation. International Journey of Psychophysiology 98:1 (2015), 35–43.
Nestor, A., Plaut, D.C., Behrmann, M., Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis. Proceedings of the Natural Academy of Sciences of the United States of America 108 (2011), 9998–10003.
Norcia, A.M., Appelbaum, L.G., Ales, J.M., Cottereau, B., Rossion, B., The steady-state visual evoked potential in vision research: a review. Journal of Vision 15(6):4 (2015), 1–46.
Oldfield, R.C., The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:1 (1971), 97–113.
Oruc, I., Barton, J.J.S., Adaptation improves discrimination of face identity. Proceedings of the Royal Society B 278 (2011), 2591–2597.
Puce, A., Allison, T., Gore, J.C., McCarthy, G., Face-sensitive regions in human extrastriate cortex studied by functional MRI. Journal of Neurophysiology 74 (1995), 1192–1199.
Regan, D., Comparison of transient and steady-state methods. Annuals of the New York Academy of Sciences 388 (1982), 45–71.
Regan, D., Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine. 1989, Elsevier.
Rhodes, G., Jeffery, L., Clifford, C.W.G., Leopold, D.A., The timecourse of higher-level face aftereffects. Vision Research 47:17 (2007), 2291–2296.
Robbins, R., McKone, E., No face-like processing for objects-of-expertise in three behavioural tasks. Cognition 103:1 (2007), 34–79.
Rolls, E.T., Representations in the brain. Synthese 129 (2001), 153–171.
Rolls, E.T., Aggelopoulos, N.C., Franco, L., Treves, A., Information encoding in the inferior temporal cortex: contributions of the firing rates and correlations between the firing of neurons. Biological Cybernetics 90 (2004), 19–32.
Rossion, B., Picture-plane inversion leads to qualitative changes of face perception. Acta Psychologica 128 (2008), 274–289.
Rossion, B., Understanding face perception by means of prosopagnosia and neuroimaging. Frontiers in Bioscience 6 (2014), 308–317 (Elite Ed.).
Rossion, B., Alonso-Prieto, E., Boremanse, A., Kuefner, D., Van Belle, G., A steady-state visual evoked potential approach to individual face perception: effect of inversion, contrast-reversal and temporal dynamics. NeuroImage 63 (2012), 1585–1600.
Rossion, B., Boremanse, A., Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. Journal of Vision 11:2 (2011), 1–21.
Rossion, B., Hanseeuw, B., Dricot, L., Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis. Brain Cognition 79 (2012), 138–157.
Rossion, B., Jacques, C., The N170 : understanding the time-course of face perception in the human brain. Luck, Kappenman, E., (eds.) The Oxford handbook of ERP components, 2011, S. Oxford University Press, 115–142.
Schiltz, C., Rossion, B., Faces are represented holistically in the human occipito-temporal cortex. NeuroImage 32 (2006), 1385–1394.
Schweinberger, S.R., Huddy, V., Burton, A.M., N250r: a face-selective brain response to stimulus repetitions. NeuroReport 15:9 (2004), 1501–1505.
Schweinberger, S.R., Pfütze, E.M., Sommer, W., Repetition priming and associative priming of face recognition: evidence from event-related potentials. Journal of Experimental Psychology – Learning, Memory, and Cognition 21:3 (1995), 722–736.
Schweinberger, S.R., Pickering, E.C., Jentzsch, I., Burton, A.M., Kaufmann, J.M., Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions. Cognitive Brain Research 14:3 (2002), 398–409.
Sergent, J., An investigation into component and configural processes underlying face perception. British Journal of Psychology 75 (1984), 221–242.
Sergent, J., Ohta, S., MacDonald, B., Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain 115 (1992), 15–36.
Srinivasan, R., Russell, D.P., Edelman, G.M., Tononi, G., Increased synchronization of neuromagnetic responses during conscious perception. Journal Neuroscience 19 (1999), 5435–5448.
Strobach, T., Carbon, C.C., Face adaptation effects: reviewing the impact of adapting information, time, and transfer. Frontiers in Perception Science, 4, 2013, 318.
Tanaka, J.W., Curran, T., Porterfield, A.L., Collins, D., Activation of preexisting and acquired face representations: the N250 event-related potential as an index of face familiarity. Journal of Cognitive Neuroscience 18:9 (2006), 1488–1497.
Tiddeman, B., Towards realism in facial image transformation: results of a wavelet MRF method. Computer Graphics Forum 24 (2005), 449–456.
Todorov, A., Pakrashi, M., Oosterhof, N.N., Evaluating faces on trustworthiness after minimal time exposure. Social Cognition 27 (2009), 813–833.
Tong, F., Nakayama, K., Robust representations for faces: evidence from visual search. Journal of Experimental Psychology: Human Perception and Performance 25 (1999), 1016–1035.
Tyler, C.W., Kaitz, M., Movement adaptation in the visual evoked response. Experimental Brain Research 27 (1977), 203–209.
Vakli, P., Németh, K., Zimmer, M., Kovács, G., The face evoked steady-state visual potentials are sensitive to the orientation, viewpoint, expression and configuration of the stimuli. International Journal of Psychophysiology 94:3 (2014), 336–350.
Valentine, T., Bruce, V., The effect of race, inversion and encoding activity upon face recognition. Acta Psychologica 61 (1986), 259–273.
Visconti di Oleggio Castello, M., Guntupalli, J.S., Yang, H., Gobbini, M.I., Facilitated detection of social cues conveyed by familiar faces. Frontiers in Human Neuroscience 8:678 (2014), 1–11.
Walter, S., Quigley, C., Andersen, S.K., Mueller, M.M., Effects of overt and covert attention on the steady-state visual evoked potential. Neuroscience Letters 519:1 (2012), 37–41.
Walther, C., Schweinberger, S.R., Kaiser, D., Kovacs, G., Neural correlates of priming and adaptation in familiar face perception. Cortex 49:7 (2013), 1963–1977.
Walther, C., Schweinberger, S.R., Kovács, G., Adaptor identity modulates adaptation effects in familiar face identification and their neural correlates. PLoS One, 8(8), 2013, e70525.
Watier, N.N., Collin, C.A., Effects of familiarity on spatial frequency thresholds for face matching. Perception 38 (2009), 1497–1507.
Webster, M.A., MacLeod, D.I.A., Visual adaptation and face perception. Philosophical Transactions of the Royal Society of London B Biological Sciences 366:1571 (2011), 1702–1725.
Weiner, K.S., Grill-Spector, K., Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. NeuroImage 52 (2010), 1559–1573.
Willis, J., Todorov, A., First impressions: making up your mind after 100 ms exposure to a face. Psychological Science 17 (2006), 592–598.
Winston, J.S., Henson, R.N.A., Fine-Goulden, M.R., Dolan, R.J., fMRI-Adaptation reveals dissociable neural representations of identity and expression in face perception. Journal of Neurophysiology 92:3 (2004), 1830–1839.
Xu, X., Yue, X., Lescroart, M.D., Biederman, I., Kim, J.G., Adaptation in the fusiform face area (FFA): image or person. Vision Research 49 (2009), 2800–2807.
Yin, R.K., Looking at upside-down faces. Journal of Experimental Psychology 81 (1969), 141–145.
Young, A.W., Hay, D.C., McWeeny, K.H., Flude, B.M., Ellis, A.W., Matching familiar and unfamiliar faces on internal and external features. Perception 14:6 (1985), 737–746.
Young, M.P., Yamane, S., Sparse population coding of faces in the inferotemporal cortex. Science 256:5061 (1992), 1327–1331.
Yovel, G., Kanwisher, N., The neural basis of the behavioral face-inversion effect. Current Biology 15 (2005), 2256–2262.
Zhen, Z., Yang, Z., Huang, L., Kong, X., Wang, X., Dang, X., et al. Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. NeuroImage 113 (2015), 13–25.