[en] Visual categorization is integral for our interaction with the natural environment. In this process, similar selective responses are produced to a class of variable visual inputs. Whether categorization is supported by partial (graded) or absolute (all-or-none) neural responses in high-level human brain regions is largely unknown. We address this issue with a novel frequency-sweep paradigm probing the evolution of face categorization responses between the minimal and optimal stimulus presentation times. In a first experiment, natural images of variable non-face objects were progressively swept from 120 to 3 Hz (8.33–333 ms duration) in rapid serial visual presentation sequences. Widely variable face exemplars appeared every 1 s, enabling an implicit frequency-tagged face-categorization electroencephalographic (EEG) response at 1 Hz. Face-categorization activity emerged with stimulus durations as brief as 17 ms (17–83 ms across individual participants) but was significant with 33 ms durations at the group level. The face categorization response amplitude increased until 83 ms stimulus duration (12 Hz), implying graded categorization responses. In a second EEG experiment, faces appeared non-periodically throughout such sequences at fixed presentation rates, while participants explicitly categorized faces. A strong correlation between response amplitude and behavioral accuracy across frequency rates suggested that dilution from missed categorizations, rather than a decreased response to each face stimulus, accounted for the graded categorization responses as found in Experiment 1. This was supported by (1) the absence of neural responses to faces that participants failed to categorize explicitly in Experiment 2 and (2) equivalent amplitudes and spatio-temporal signatures of neural responses to behaviorally categorized faces across presentation rates. Overall, these observations provide original evidence that high-level visual categorization of faces, starting at about 100 ms following stimulus onset in the human brain, is variable across observers tested under tight temporal constraints, but occurs in an all-or-none fashion.
Adrian, E.D., Matthews, B.H.C., The Berger rhythm: potential changes from the occipital lobes in man. Brain 4:57 (1934), 355–385.
Allison, T., Ginter, H., McCarthy, G., Nobre, A.C., Puce, A., Luby, M., Spencer, D.D., Face recognition in human extrastriate cortex. J. Neurophysiol. 71:2 (1994), 821–825.
Bachman, T., On the all-or-none rule of conscious perception. Front. Hum. Neurosci., 7, 2013, 387.
Bacon-Macé, N., Macé, M.J., Fabre-Thorpe, M., Thorpe, S.J., The time course of visual processing: backward masking and natural scene categorisation. Vis. Res. 45:11 (2005), 1459–1469.
Bar, M., Tootell, R.B.H., Schacter, D.L., Greve, D.N., Fischl, B., Mendola, J.D., Rosen, B.R., Dale, A.M., Cortical mechanisms specific to explicit visual object recognition. Neuron 29:2 (2001), 529–535.
Breitmeyer, B.G., Visual Masking: an Integrative Approach. 1984, Oxford University Press, Oxford.
Bruce, V., Young, A., In the Eye of the Beholder: the Science of Face Perception. 1998, Oxford University Press, New York, NY, US.
Bushnell, I.W.R., Mother's face recognition in newborn infants: learning and memory. Infant Child Dev. 10 (2001), 67–74.
Caharel, S., Leleu, A., Bernard, C., Viggiano, M.P., Lalonde, R., Rebaï, M., Early holistic face-like processing of Arcimboldo paintings in the right occipito-temporal cortex: evidence from the N170 ERP component. Int. J. Psychophysiol. 90 (2013), 157–164.
Carandini, M., Demb, J.B., Mante, V., Tolhurst, D.J., Dan, Y., Olshausen, B.A., et al. Do we know what the early visual system does?. J. Neurosci. 25 (2005), 10577–10597.
Christensen, M.S., Ramsøy, T.Z., Lund, T.E., Madsen, K.H., Rowe, J.B., An fMRI study of the neural correlates of graded visual perception. Neuroimage 31 (2006), 1711–1725.
Cichy, R.M., Pantazis, D., Oliva, A., Resolving human object recognition in space and time. Nat. Neurosci. 17:3 (2014), 455–462.
Crouzet, S.M., Thorpe, S.J., Low-level cues and ultra-fast face detection. Front. Psychol., 2, 2011, 342.
Crouzet, S.M., Kirchner, H., Thorpe, S.J., Fast saccades toward faces: face detection in just 100 ms. J. Vis., 10, 2010, 3.
de Gardelle, V., Charles, L., Kouider, S., Perceptual awareness and categorical representation of faces: evidence from masked priming. Conscious. Cognit.: Int. J. 20:4 (2011), 1272–1281.
Del Cul, A., Baillet, S., Dehaene, S., Brain dynamics underlying the nonlinear threshold for access to consciousness. PLoS Biol., 5(10), 2007, e260.
Dzhelyova, M., Rossion, B., The effect of parametric stimulus size variation on individual face discrimination indexed by fast periodic visual stimuliation. BMC Neurosci. 15:87 (2014), 1–12.
Edelman, G.M., Group selecting and phasic reenterant signalling : a theory a higher brain function. The Mindful Brain, 1978, MIT Press, Cambridge, MA, 51–100.
Edelman, G.M., Neural Darwinism: the Theory of Neuronal Group Selection. 1987, MIT Press, Cambridge, MA.
Enns, J.T., Di Lollo, V., What's new in visual masking?. Trends Cognit. Sci. 4 (2000), 345–352.
Fisch, L., Privman, E., Ramot, M., Harel, M., Nir, Y., Kipervasser, S., Andelman, F., et al. Neural “ignition”: enhanced activation linked to perceptual awareness in human ventral stream visual cortex. Neuron 64 (2009), 562–574.
Foldiak, P., Xiao, D., Keysers, C., Edwards, R., Perrett, D.I., Rapid serial visual presentation for the determination of neural selectivity in area STSa. Prog. Brain Res. 144 (2004), 107–116.
Gao, X., Gentile, F., Rossion, B., Fast periodic stimulation: a highly effective approach in fMRI brain mapping. Brain Struct. Funct. 223 (2018), 2433–2454.
Goldstone, R.L., Kersten, A., Carvalho, P.F., Categorization and concepts. Wixted, J.T., (eds.) Stevens’ Handbook of Experimental Psychology and Cognitive Neuroscience, 2018, 10.1002/9781119170174.epcn308.
Grill-Spector, K., Kanwisher, N., Visual recognition: as soon as you know it's there, you know what it is. Psychol. Sci. 16:2 (2005), 152–160.
Grill-Spector, K., Kushnir, T., Hendler, T., Malach, R., The dynamics of object-selective activation correlate with recognition performance in humans. Nat. Neurosci. 3:8 (2000), 837–843.
Grill-Spector, K., Weiner, K.S., Kay, K., Gomez, J., The functional neuroanatomy of human face perception. Ann. Rev. Vis. Sci. 3 (2017), 167–196.
Harris, J.A., Wu, C.T., Woldorff, M.G., Sandwich masking eliminates both visual awareness of faces and face-specific brain activity through a feedforward mechanism. J. Vis., 11(7), 2011, 10.
Helmholtz, H., Handbuch der physiologischen Optik. Karsten, G., (eds.) Allgemeine Encyklopddie der Physik, vol. 9, 1867, Voss), Leipzig.
Herrmann, C.S., Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp. Brain Res. 137 (2001), 346–353.
Herschler, O., Hochstein, S., At first sight: a high-level pop out effect for faces. Vis. Res. 45:13 (2005), 1707–1724.
Horovitz, S.G., Rossion, B., Skudlarski, P., Gore, J.C., Parametric design and correlational analyses help integrating fMRI and electrophysiological data during face processing. Neuroimage 22 (2004), 1587–1595.
Jacques, C., Retter, T.L., Rossion, B., A single glance at a face generates larger and qualitatively different category-selective spatio-temporal signatures than other ecologically-relevant categories in the human brain. Neuroimage 137 (2016), 21–33.
Jacques, C., Witthoft, N., Weiner, K.S., Foster, B.L., Rangarajan, V., Hermes, D., et al. Corresponding ECoG and fMRI category-selective signals in human ventral temporal cortex. Neuropsychologia 83 (2016), 14–28.
Jemel, B., Schuller, A.-M., Cheref-Khan, Y., Goffaux, V., Crommelinck, M., Raymond, B., Stepwise emergence of the face-sensitive N170 event-related potential component. Cognit. Neurosci. Neuropsychol. 14:16 (2003), 2035–2039.
Johnson, M.H., Dziurawiec, S., Ellis, H., Morton, J., Newborns’ preferential tracking of face-like stimuli and its subsequent decline. Cognition 40:1–2 (1991), 1–19.
Jonas, J., Jacques, C., Liu-Shuang, J., Brissart, H., Colnat-Coulbois, S., Maillard, L., Rossion, B., A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials. Proc. Natl. Acad. Sci. U.S.A. 113 (2016), E4088–E4097.
Kanwisher, N., McDermott, J., Chun, M.M., The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17 (1997), 4302–4311.
Keysers, C., Xiao, D.-K., Földiák, P., Perrett, D.I., The speed of sight. J. Cognit. Neurosci. 13 (2001), 90–101.
Keysers, C., Xiao, D.-K., Foldiak, P., Perrett, D.I., Out of sight but not out of mind: the neurophysiology of iconic memory in the superior temporal sulcus. Cogn. Neuropsychol. 22:3–4 (2005), 316–332.
Kleinschmidt, A., Buchel, C., Zeki, S., Frackowiak, R.S.J., Human brain activity during spontaneously reversing perception of ambiguous figures. Proc. Roy. Soc. Lond. B, 265, 1998, 1413.
Koch, C., Massimini, M., Boly, M., Tononi, G., Neural correlates of consciousness: progress and problems. Nat. Rev. Neurosci. 17:5 (2016), 307–321.
Kovács, G., Vogels, R., Orban, G.A., Cortical correlate of pattern backward masking. PNAS USA 92:12 (1995), 5587–5591.
Lee, I.A., Preacher, K.J., Calculation for the test of the difference between two dependent correlations with one variable in common [Computer software]. Available from: http://quantpsy.org, 2013, September.
Leleu, A., Rekow, D., Poncet, F., et al. Maternal odor shapes rapid face categorization in the infant brain. Dev. Sci., 2019, e12877.
Liu, H., Agam, Y., Madsen, J.R., Kreiman, G., Timing, timing, timing: fast decoding of object information from intracranial field potentials in human visual cortex. Neuron 62:2 (2009), 281–290.
Luck, S.J., An Introduction to the Event-Related Potential Technique. 2005, MIT Press, Cambridge, MA.
Maguire, J.F., Howe, P.D.L., Failure to detect meaning in RSVP at 27 ms per picture. Atten. Percept. Psychophys., 78, 2016, 1405.
Marti, S., Dehaene, S., Discrete and continuous mechanisms of temporal selection in rapid visual streams. Nat. Commun. 8 (2017), 1–13 1955.
McCarthy, G., Wood, C.C., Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr. Clin. Neurophysiology Evoked Potentials Sect. 62 (1985), 203–208.
Mohsenzadeh, Y., Qin, S., Cichy, R.M., Pantazis, D., Ultra-Rapid serial visual presentation reveals dynamics of feedforward and feedback processes in the ventral visual pathway. eLife, 7, 2018, e36329.
Moutoussis, K., Zeki, S., The relationship between cortical activation and perception investigated with invisible stimuli. PNAS USA 99:14 (2002), 9527–9532.
Murphy, G.L., The Big Book of Concepts. 2002, MIT Press, Cambridge, MA.
Navajas, J., Ahmadi, M., Quian Quiroga, R., Uncovering the mechanisms of conscious face perception: a single-trial study of the n170 responses. J. Neurosci. 33 (2013), 1337–1343.
Navajas, J., Rey, H.G., Quiroga, R.Q., Perceptual and contextual awareness: methodological considerations in the search for the neural correlates of consciousness. Front. Psychol., 5, 2014, 959.
Norcia, A.M., Appelbaum, L.G., Ales, J.M., Cottereau, B., Rossion, B., The steady-state visual evoked potential in vision research: a review. J. Vis. 15:6 (2015), 1–46 4.
Nunez, P.L., Srinivasan, R., Electric Fields of the Brain. 2006, Oxford University Press, Oxford.
Omer, Y., Sapir, R., Hatuka, Y., Yovel, G., What is a face? Critical features for face detection. Perception 48 (2019), 437–446.
Oostenveld, R., Praamstra, P., The Five Percent Electrode System for High-Resolution EEG and ERP Measurements, vol. 112, 2001, 713–719 4.
Or, C.C.-F, Retter, T.L., Rossion, B., The contribution of color information to rapid face categorization in natural scenes. J. Vis. 19:5 (2019), 1–20.
Perrett, D.I., Seeing the future: natural image sequences produce “anticipatory” neuronal activity and bias perceptual report. Q. J. Exp. Psychol. 62:11 (2009), 2081–2104.
Potter, M.C., Recognition and memory for briefly presented scenes. Front. Psychol., 3, 2012, 32.
Potter, M.C., Levy, E.I., Recognition memory for a rapid sequence of pictures. J. Exp. Psychol. 81 (1969), 10–15.
Potter, M.C., Wyble, B., Hagmann, C.E., McCourt, E.S., Detecting meaning in RSVP at 13 ms per picture. Atten. Percept. Psychophys. 76:2 (2014), 270–279.
Puce, A., Allison, T., Gore, J.C., McCarthy, G., Face-sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol. 74:3 (1995), 1192–1199.
Quek, G.L., Liu-Shuang, J., Goffaux, V., Rossion, B., Ultra-coarse, single glance face detection in a dynamic visual stream. NeuroImage 176 (2018), 465–476.
Quek, G., Rossion, B., Category-selective human brain processes elicited in fast periodic visual stimulation streams are immune to temporal predictability. Neuropsychologia 104 (2017), 182–200.
Quiroga, R.Q., Mukamel, R., Isham, E.A., Malach, R., Fried, I., Human single-neuron responses at the threshold of conscious recognition. Proc. Natl. Acad. Sci. Unit. States Am. 105:9 (2008), 3599–3604.
Regan, D., Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine. 1989, Elsevier, Amsterdam, the Netherlands.
Retter, T.L., Rossion, B., Uncovering the neural magnitude and spatio-temporal dynamics of natural image categorization in a fast visual stream. Neuropsychologia 91 (2016), 9–28.
Retter, T.L., Jiang, F., Webster, M.A., Rossion, B., Dissociable effects of inter-stimulus interval and presentation duration on rapid face categorization. Vis. Res. 145 (2018), 11–20.
Retter, T.L., Rossion, B., Visual adaptation reveals an objective electrophysiological measure of high-level individual face discrimination. Sci. Rep. 7:3269 (2017), 1–10.
Rolls, E.T., Tovée, M.J., Processing Speed in the Cerebral Cortex and the. 1994.
Rossion, B., Torfs, K., Jacques, C., Liu-Shuang, J., Fast periodic presentation of natural face images reveals a robust face-selective electrophysiological response in the human brain. J. Vis. 15:1 (2015), 1–18.
Rouder, J.N., Speckman, P.L., Sun, D., Morey, R.D., Iverson, G., Bayesian t-tests for accepting and rejecting the null hypothesis. Psychon. Bull. Rev. 16 (2009), 225–237.
Rousselet, G.A., Macé, M.J.-M., Fabre-Thorpe, M., Is it an animal? Is it a human face? Fast processing in upright and inverted natural scenes. J. Vis., 3(6), 2003, 5.
Rousselet, G.A., Pernet, C.R., Bennett, P.J., Sekuler, A.B., Parametric study of EEG sensitivity to phase noise during face processing. BMC Neurosci., 9, 2008, 98.
Scheirer, W.J., Anthony, S.E., Nakayama, K., Cox, D.D., Perceptual annotation: measuring human vision to improve computer vision. IEEE Trans. Pattern Anal. Mach. Intell. 36:8 (2014), 1679–1686.
Sekar, K., Findley, W.M., Linas, R.R., Evidence for an all-or-none perceptual response: single-trial analyses of magnetoencephalography signals indicate an abrupt transition between visual perception and its absence. Neuroscience 206 (2012), 167–182.
Sekar, K., Findley, W.M., Poeppel, D., Llinás, R.R., Cortical response tracking the conscious experience of threshold duration visual stimuli indicates visual perception is all or none. Proc. Natl. Acad. Sci. U. S. A. 110:14 (2013), 5642–5647.
Sergent, J., Ohta, S., MacDonald, B., Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain 115:1 (1992), 15–36.
Shafto, J.P., Pitts, M.A., Neural signatures of conscious face perception in an inattentional blindness paradigm. J. Neurosci. 35 (2015), 10940–10948.
Smith, E.E., Medin, D.L., Categories and Concepts. 1981, Harvard University Press, Cambridge, MA.
Sugden, N.A., Mohamed-Ali, I., Moulson, M.C., I spy with my little eye: typical, daily exposure to faces documented from a first-person infant perspective. Dev. Psychobiol. 56:2 (2014), 249–261.
Tanskanen, T., Näsänen, R., Ojanpää, H., Hari, R., Face recognition and cortical responses: effect of stimulus duration. Neuroimage 35 (2007), 1636–1644.
Thorpe, S.J., Fize, D., Marlot, C., Speed of processing in the human visual system. Nature 381:6582 (1996), 520–522.
Townsend, J.T., Ashby, F.G., The Stochastic Modeling of Elementary Psychological Processes. 1983, Cambridge University Press, Cambridge.
Tsuchiya, N., Wilke, M., Frässle, S., Lamme, V.A., No-report paradigms: extracting the true neural correlates of consciousness. Trends Cognit. Sci. 19 (2015), 757–770.
Vanni, S., Revonsuo, A., Saarinen, J., Hari, R., Visual awareness of objects correlates with activity of right occipital cortex. Neuroreport 8:1 (1996), 183–186.
Wilmer, J.B., Germine, L.T., Nakayama, K., Face recognition: a model specific ability. Front. Hum. Neurosci. 8:769 (2014), 1–5.
Windey, B., Cleeremans, A., Consciousness as a graded and an all-or-none phenomenon: a conceptual analysis. Conscious. Cognit. 35 (2015), 185–191.
Windey, B., Vermeiren, A., Atas, A., Cleeremans, A., The graded and dichotomous nature of visual awareness. Phil. Trans. R. Soc. B, 369, 2014, 20130282.
Woodman, G.F., A brief introduction to the use of event-related potentials in studies of perception and attention. Atten. Percept. Psychophys. 72:8 (2010), 2031–2046.
Xu, B., Liu-Shuang, J., Rossion, B., Tanaka, J., Individual differences in face identity processing with fast periodic visual stimulation. J. Cognit. Neurosci. 29:8 (2017), 1368–1377.
Yovel, G., Wilmer, J.B., Duchaine, B., What can individual differences reveal about face processing?. Front. Hum. Neurosci. 8:562 (2014), 1–9.
Zhen, Z., Yang, Z., Huang, L., Kong, X.-z., Wang, X., Dang, X., et al. Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. Neuroimage 113 (2015), 13–25.
