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Visual adaptation reveals an objective electrophysiological measure of high-level individual face discrimination

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Retter, Talia [UCL] Rossion, Bruno [UCL]

The ability to individualize faces is a fundamental human brain function. Following visual adaptation to one individual face, the suppressed neural response to this identity becomes discriminable from an unadapted facial identity at a neural population level. Here, we investigate a simple and objective measure of individual face discrimination with electroencephalographic (EEG) frequency tagging following adaptation. In a first condition, (1) two facial identities are presented in alternation at a rate of six images per second (6 Hz; 3 Hz identity repetition rate) for a 20 s testing sequence, following 10-s adaptation to one of the facial identities; this results in a significant identity discrimination response at 3 Hz in the frequency domain of the EEG over right occipito-temporal channels, replicating our previous findings. Such a 3 Hz response is absent for two novel conditions, in which (2) the faces are inverted and (3) an identity physically equidistant from the two faces is adapted. These results indicate that low-level visual features present in inverted or unspecific facial identities are not sufficient to produce the adaptation effect found for upright facial stimuli, which appears to truly reflect identity-specific perceptual representations in the human brain.

Document type Article de périodique (Journal article)
Access type Accès restreint
Publication date 2017
Language Anglais
Journal information "Scientific Reports" - Vol. 7, p. 7-12 (2017)
Peer reviewed yes
Publisher Springer Nature
Publication status Publié
Affiliations UCL - SSH/IPSY - Psychological Sciences Research Institute
UCL - SSS/IONS - Institute of NeuroScience
UCL - SSS/IONS/COSY - Systems & cognitive Neuroscience
Keywords Multidisciplinary
Links
  1. Rossion Bruno, Understanding face perception by means of prosopagnosia and neuroimaging, 10.2741/e706
  2. Dubois J., de Berker A. O., Tsao D. Y., Single-Unit Recordings in the Macaque Face Patch System Reveal Limitations of fMRI MVPA, 10.1523/jneurosci.4037-14.2015
  3. Grill-Spector Kalanit, Malach Rafael, fMR-adaptation: a tool for studying the functional properties of human cortical neurons, 10.1016/s0001-6918(01)00019-1
  4. Gentile Francesco, Rossion Bruno, Temporal frequency tuning of cortical face-sensitive areas for individual face perception, 10.1016/j.neuroimage.2013.11.053
  5. Grotheer Mareike, Hermann Petra, Vidnyánszky Zoltán, Kovács Gyula, Repetition probability effects for inverted faces, 10.1016/j.neuroimage.2014.08.006
  6. Davies-Thompson Jodie, Gouws André, Andrews Timothy J., An image-dependent representation of familiar and unfamiliar faces in the human ventral stream, 10.1016/j.neuropsychologia.2009.01.017
  7. Walther Christian, Schweinberger Stefan R., Kaiser Daniel, Kovács Gyula, Neural correlates of priming and adaptation in familiar face perception, 10.1016/j.cortex.2012.08.012
  8. Caharel Stéphanie, d’Arripe Olivier, Ramon Meike, Jacques Corentin, Rossion Bruno, Early adaptation to repeated unfamiliar faces across viewpoint changes in the right hemisphere: Evidence from the N170 ERP component, 10.1016/j.neuropsychologia.2008.11.016
  9. Jacques, C., d’Arripe, O. & Rossion, B. The time course of the inversion effect during individual face discrimination. Journal of Vision 7(8):3, 1–9 (2007).
  10. Schweinberger Stefan R, Pickering Esther C, Jentzsch Ines, Burton A.Mike, Kaufmann Jürgen M, Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions, 10.1016/s0926-6410(02)00142-8
  11. Henson R.N.A, Rugg M.D, Neural response suppression, haemodynamic repetition effects, and behavioural priming, 10.1016/s0028-3932(02)00159-8
  12. Feuerriegel Daniel, Selecting appropriate designs and comparison conditions in repetition paradigms, 10.1016/j.cortex.2015.10.022
  13. Retter Talia L., Rossion Bruno, Visual adaptation provides objective electrophysiological evidence of facial identity discrimination, 10.1016/j.cortex.2015.11.025
  14. Rossion Bruno, Understanding individual face discrimination by means of fast periodic visual stimulation, 10.1007/s00221-014-3934-9
  15. 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):8, 1–13 (2009).
  16. Tyler C.W., Kaitz M., Movement adaptation in the visual evoked response, 10.1007/bf00237698
  17. Regan, D. Human Brain Electrophysiology. New York (Elsevier, 1989).
  18. 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, 1–46 (2015).
  19. Robbins Rachel, McKone Elinor, No face-like processing for objects-of-expertise in three behavioural tasks, 10.1016/j.cognition.2006.02.008
  20. Freire Alejo, Lee Kang, Symons Lawrence A, The Face-Inversion Effect as a Deficit in the Encoding of Configural Information: Direct Evidence, 10.1068/p3012
  21. Yin Robert K., Looking at upside-down faces., 10.1037/h0027474
  22. Rossion Bruno, Picture-plane inversion leads to qualitative changes of face perception, 10.1016/j.actpsy.2008.02.003
  23. Rossion Bruno, Distinguishing the cause and consequence of face inversion: The perceptual field hypothesis, 10.1016/j.actpsy.2009.08.002
  24. Liu-Shuang Joan, Norcia Anthony M., Rossion Bruno, An objective index of individual face discrimination in the right occipito-temporal cortex by means of fast periodic oddball stimulation, 10.1016/j.neuropsychologia.2013.10.022
  25. Rhodes Gillian, Evangelista Emma, Jeffery Linda, Orientation-sensitivity of face identity aftereffects, 10.1016/j.visres.2009.07.010
  26. Leopold David A., O'Toole Alice J., Vetter Thomas, Blanz Volker, Prototype-referenced shape encoding revealed by high-level aftereffects, 10.1038/82947
  27. Webster M. A., MacLeod D. I. A., Visual adaptation and face perception, 10.1098/rstb.2010.0360
  28. Grill-Spector Kalanit, Henson Richard, Martin Alex, Repetition and the brain: neural models of stimulus-specific effects, 10.1016/j.tics.2005.11.006
  29. Tiddeman, B., Stirrat, M. & Perrett, D. Twards realism in facial transformation: results of a wavelet MRF method. Computer Graphics Forum. Eurographics conference issue 24, 1–5 (2005).
  30. Tanaka J, Mapping attractor fields in face space: the atypicality bias in face recognition, 10.1016/s0010-0277(98)00048-1
  31. Bentin Shlomo, Allison Truett, Puce Aina, Perez Erik, McCarthy Gregory, Electrophysiological Studies of Face Perception in Humans, 10.1162/jocn.1996.8.6.551
  32. Rossion Bruno, Jacques Corentin, The N170: Understanding the Time Course of Face Perception in the Human Brain, 10.1093/oxfordhb/9780195374148.013.0064
  33. Jonas Jacques, Jacques Corentin, Liu-Shuang Joan, Brissart Hélène, Colnat-Coulbois Sophie, Maillard Louis, Rossion Bruno, A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials, 10.1073/pnas.1522033113
  34. SERGENT JUSTINE, OHTA SHINSUKE, MACDONALD BRENNAN, FUNCTIONAL NEUROANATOMY OF FACE AND OBJECT PROCESSING : A POSITRON EMISSION TOMOGRAPHY STUDY, 10.1093/brain/115.1.15
  35. Frässle Stefan, Krach Sören, Paulus Frieder Michel, Jansen Andreas, Handedness is related to neural mechanisms underlying hemispheric lateralization of face processing, 10.1038/srep27153
  36. Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: A module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 17(11), 4302–4311 (1997).
  37. Sergent Justine, Signoret Jean-Louis, Varieties of Functional Deficits in Prosopagnosia, 10.1093/cercor/2.5.375
  38. Meadows J. C., The anatomical basis of prosopagnosia, 10.1136/jnnp.37.5.489
  39. HECAEN H., ANGELERGUES R., Agnosia for Faces (Prosopagnosia), 10.1001/archneur.1962.04210020014002
  40. Retter Talia L., Rossion Bruno, Uncovering the neural magnitude and spatio-temporal dynamics of natural image categorization in a fast visual stream, 10.1016/j.neuropsychologia.2016.07.028
  41. 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, 897–904 (2005).
  42. Schweinberger Stefan R., Neumann Markus F., Repetition effects in human ERPs to faces, 10.1016/j.cortex.2015.11.001
  43. Alonso-Prieto Esther, Belle Goedele Van, Liu-Shuang Joan, Norcia Anthony M., Rossion Bruno, The 6Hz fundamental stimulation frequency rate for individual face discrimination in the right occipito-temporal cortex, 10.1016/j.neuropsychologia.2013.08.018
  44. Hsiao Janet Hui-wen, Cottrell Garrison, Two Fixations Suffice in Face Recognition, 10.1111/j.1467-9280.2008.02191.x
  45. Todorov Alexander, Pakrashi Manish, Oosterhof Nikolaas N., Evaluating Faces on Trustworthiness After Minimal Time Exposure, 10.1521/soco.2009.27.6.813
  46. Willis Janine, Todorov Alexander, First Impressions : Making Up Your Mind After a 100-Ms Exposure to a Face, 10.1111/j.1467-9280.2006.01750.x
  47. de Heering Adélaïde, Rossion Bruno, Rapid categorization of natural face images in the infant right hemisphere, 10.7554/elife.06564
  48. Lochy Aliette, Van Reybroeck Marie, Rossion Bruno, Left cortical specialization for visual letter strings predicts rudimentary knowledge of letter-sound association in preschoolers, 10.1073/pnas.1520366113
  49. Pei, F., Bldassi, S. & Norcia, A. M. Electrophysiological measures of low-level vision reveal spatial processing deficits and hemispheric asymmetry in autism spectrum disorder. Journal of Vision 14(11):3, 1–12 (2014).
  50. Oldfield R.C., The assessment and analysis of handedness: The Edinburgh inventory, 10.1016/0028-3932(71)90067-4
  51. Benton A.L., Van Allen M.W., Prosopagnosia and facial discrimination, 10.1016/0022-510x(72)90004-4
  52. 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):16, 1–21 (2011).
  53. Dzhelyova, M. & Rossion, B. The effect of parametric stimulus size variation on individual face discrimination indexed by fast periodic visual stimuliation. BMC Neuroscience 15(87), 1–12 (2014).
  54. Oostenveld Robert, Praamstra Peter, The five percent electrode system for high-resolution EEG and ERP measurements, 10.1016/s1388-2457(00)00527-7
  55. Rossion B., Torfs K., Jacques C., Liu-Shuang J., Fast periodic presentation of natural images reveals a robust face-selective electrophysiological response in the human brain, 10.1167/15.1.18
  56. Rossion Bruno, Prieto Esther Alonso, Boremanse Adriano, Kuefner Dana, Van Belle Goedele, A steady-state visual evoked potential approach to individual face perception: Effect of inversion, contrast-reversal and temporal dynamics, 10.1016/j.neuroimage.2012.08.033
  57. Srinivasan, R., Russell, D. P., Edelman, G. M. & Tononi, G. Increased synchronization of neuromagnetic responses during conscious perception. Journal Neuroscience 19, 5435–5448 (1999).
  58. Jacques, C., d’Arripe, O. & Rossion, B. The time course of the inversion effect during individual face discrimination. Journal of Vision 7(8):3, 1–9 (2007).
Bibliographic reference Retter, Talia ; Rossion, Bruno. Visual adaptation reveals an objective electrophysiological measure of high-level individual face discrimination. In: Scientific Reports, Vol. 7, p. 7-12 (2017)
Permanent URL http://hdl.handle.net/2078.1/195444