A single glance at natural face images generate larger and qualitatively different category-selective spatio-temporal signatures than other ecologically-relevant categories in the human brain.
[en] Although humans discriminate natural images of faces from other categories at a single glance, clarifying the neural specificity and spatio-temporal dynamics of this process without low-level visual confounds remains a challenge. We recorded high-density scalp electroencephalogram while presenting natural images of various objects at a fast periodic rate (5.88images/s). In different stimulation sequences, numerous variable exemplars of three categories associated with cortical specialization in neuroimaging - faces, body parts, or houses - appeared every five images (5.88Hz/5=1.18Hz). In these fast periodic visual stimulation (FPVS) sequences, common low- and high-level visual processes between these categories and other objects are captured at the 5.88Hz frequency, while high-level category-selective responses are objectively quantified at the 1.18Hz frequency and harmonics. Category-selective responses differed quantitatively and qualitatively between faces, body parts and houses. First, they were much larger (2-4 times) for faces over the whole scalp. Second, specific and reliable scalp topographical maps of category-selective responses pointed to distinct principle neural sources for faces (ventral occipito-temporal), body parts (lateral occipito-temporal) and houses (dorso-medial occipital). Category-selective EEG responses were found at multiple time-windows from 110 to 600ms post-stimulus onset. Faces elicited the most complex spatio-temporal profile with up to four selective responses, although body parts and houses also elicited selective responses more complex than previously described. These observations indicate that a single glance at natural face images inserted in a rapid stream of natural objects generates a quantitatively and qualitatively unique category-selective spatio-temporal signature in occipito-temporal cortical areas of the human brain.
Disciplines :
Neurosciences & behavior
Author, co-author :
Jacques, Corentin; Psychological Sciences Research Institute (IPSY), University of Louvain, 1348 Louvain-la-Neuve, Belgium, Institute of Neuroscience, University of Louvain, 1348 Louvain-la-Neuve, Belgium
RETTER, Talia ; Psychological Sciences Research Institute (IPSY), University of Louvain, 1348 Louvain-la-Neuve, Belgium, Institute of Neuroscience, University of Louvain, 1348 Louvain-la-Neuve, Belgium, Department of Psychology/296, University of Nevada, Reno, NV 89557, United States
Rossion, Bruno; Psychological Sciences Research Institute (IPSY), University of Louvain, 1348 Louvain-la-Neuve, Belgium, Institute of Neuroscience, University of Louvain, 1348 Louvain-la-Neuve, Belgium. Electronic address: bruno.rossion@uclouvain.be
External co-authors :
yes
Language :
English
Title :
A single glance at natural face images generate larger and qualitatively different category-selective spatio-temporal signatures than other ecologically-relevant categories in the human brain.
Belgian Federal Science Policy Office Belgian National Fund for Scientific Research European Research Council
Funding text :
The authors thank two anonymous reviewers for their constructive critical comments on a previous version of this manuscript. CJ is supported by the Belgian Federal Science Policy Office (BELSPO, return grant 2012 ). BR and TR are supported by the Belgian National Fund for Scientific Research (Fonds de la Recherche Scientifique; FNRS) . This work was supported by a grant from the European Research Council (ERC, facessvep 284025 ). Authors declare no competing interest.
Allison T., Puce A., Spencer D., McCarthy G., Belger A. Electrophysiological studies of human face perception. I: potential generated in occipitotemporal cortex by face and non-face stimuli. Cereb. Cortex 1999, 9:415-430.
Astafiev S.V., Stanley C.M., Shulman G.L., Corbetta M. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat. Neurosci. 2004, 7:542-548. 10.1038/nn1241.
Avidan G., Behrmann M. Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Curr. Biol. 2009, 19:1146-1150. 10.1016/j.cub.2009.04.060.
Axelrod V., Yovel G. The challenge of localizing the anterior temporal face area: a possible solution. NeuroImage 2013, 81:371-380. 10.1016/j.neuroimage.2013.05.015.
Bastin J., Vidal J.R., Bouvier S., Perrone-Bertolotti M., Bénis D., Kahane P., David O., Lachaux J.-P., Epstein R.A. Temporal components in the parahippocampal place area revealed by human intracerebral recordings. J. Neurosci. 2013, 33:10123-10131. 10.1523/JNEUROSCI.4646-12.2013.
Bentin S., McCarthy G., Perez E., Puce A., Allison T. Electrophysiological studies of face perception in humans. J. Cogn. Neurosci. 1996, 8:551-565.
Busigny T., Graf M., Mayer E., Rossion B. Acquired prosopagnosia as a face-specific disorder: ruling out the general visual similarity account. Neuropsychologia 2010, 48:2051-2067. 10.1016/j.neuropsychologia.2010.03.026.
Carlson T., Tovar D.A., Kriegeskorte N. Representational dynamics of object vision: the first 1000ms. J. Vis. 2013, 13(10):1-19. (1). 10.1167/13.10.1.
Cauchoix M., Barragan-Jason G., Serre T., Barbeau E.J. The neural dynamics of face detection in the wild revealed by MVPA. J. Neurosci. 2014, 34:846-854. 10.1523/JNEUROSCI.3030-13.2014.
Cichy R.M., Pantazis D., Oliva A. Resolving human object recognition in space and time. Nat. Neurosci. 2014, 17:455-462. 10.1038/nn.3635.
Crouzet S.M., Thorpe S.J. Fast saccades toward faces: face detection in just 100ms. J. Vis. 2010, 10(4):1-17. (16). 10.1167/10.4.16.
Crouzet S.M., Thorpe S.J. Low-level cues and ultra-fast face detection. Front. Psychol. 2011, 2:342. 10.3389/fpsyg.2011.00342.
de Heering A., Rossion B. Rapid categorization of natural face images in the infant right hemisphere. Elife 2015, 4. 10.7554/eLife.06564.
Dilks D.D., Julian J.B., Paunov A.M., Kanwisher N. The occipital place area is causally and selectively involved in scene perception. J. Neurosci. 2013, 33:1331-1336. 10.1523/JNEUROSCI.4081-12.2013.
Downing P.E., Jiang Y., Shuman M., Kanwisher N. A cortical area selective for visual processing of the human body. Science 2001, 293:2470-2473. 10.1126/science.1063414.
Downing P.E., Chan A.W.-Y., Peelen M.V., Dodds C.M., Kanwisher N. Domain specificity in visual cortex. Cereb. Cortex 2006, 16:1453-1461. 10.1093/cercor/bhj086.
Dzhelyova M., Rossion B. Supra-additive contribution of shape and surface information to individual face discrimination as revealed by fast periodic visual stimulation. J. Vis. 2014, 14(14):15. 10.1167/14.14.15.
Eimer M. The face-specific N170 component reflects late stages in the structural encoding of faces. Neuroreport 2000, 11:2319-2324.
Engell A.D., McCarthy G. Face, eye, and body selective responses in fusiform gyrus and adjacent cortex: an intracranial EEG study. Front. Hum. Neurosci. 2014, 8:642. 10.3389/fnhum.2014.00642.
Epstein R., Kanwisher N. A cortical representation of the local visual environment. Nature 1998, 392:598-601. 10.1038/33402.
Epstein R., Harris A., Stanley D., Kanwisher N. The parahippocampal place area: recognition, navigation, or encoding?. Neuron 1999, 23:115-125.
Ganis G., Smith D., Schendan H.E. The N170, not the P1, indexes the earliest time for categorical perception of faces, regardless of interstimulus variance. NeuroImage 2012, 62:1563-1574. 10.1016/j.neuroimage.2012.05.043.
Gobbini M.I., Haxby J.V. Neural systems for recognition of familiar faces. Neuropsychologia 2007, 45:32-41. 10.1016/j.neuropsychologia.2006.04.015.
Goffaux V., Gauthier I., Rossion B. Spatial scale contribution to early visual differences between face and object processing. Cogn. Brain Res. 2003, 16:416-424.
Grefkes C., Fink G.R. The functional organization of the intraparietal sulcus in humans and monkeys. J. Anat. 2005, 207:3-17. 10.1111/j.1469-7580.2005.00426.x.
Grill-Spector K. The neural basis of object perception. Curr. Opin. Neurobiol. 2003, 13:159-166. 10.1016/S0959-4388(03)00040-0.
Grill-Spector K., Weiner K.S. The functional architecture of the ventral temporal cortex and its role in categorization. Nat. Rev. Neurosci. 2014, 15:536-548. 10.1038/nrn3747.
Grill-Spector K., Kourtzi Z., Kanwisher N. The lateral occipital complex and its role in object recognition. Vis. Res. 2001, 41:1409-1422.
Halgren E., Raij T., Marinkovic K., Jousmaki V., Hari R. Cognitive response profile of the human fusiform face area as determined by MEG. Cereb. Cortex 2000, 10:69-81.
Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 2000, 4:223-233.
Hershler O., Hochstein S. At first sight: a high-level pop out effect for faces. Vis. Res. 2005, 45:1707-1724.
Hershler O., Hochstein S. With a careful look: still no low-level confound to face pop-out. Vis. Res. 2006, 46:3028-3035. 10.1016/j.visres.2006.03.023.
Hershler O., Golan T., Bentin S., Hochstein S. The wide window of face detection. J. Vis. 2010, 10:21. 10.1167/10.10.21.
Honey C., Kirchner H., VanRullen R. Faces in the cloud: Fourier power spectrum biases ultrarapid face detection. J. Vis. 2008, 8(12):1-13. (9). 10.1167/8.12.9.
Itier R.J., Taylor M.J. N170 or N1? Spatiotemporal differences between object and face processing using ERPs. Cereb. Cortex 2004, 14:132-142. 10.1093/cercor/bhg111.
Jacques C., Witthoft N., Weiner K.S., Foster B.L., Rangarajan V., Hermes D., Miller K.J., Parvizi J., Grill-Spector K. Corresponding ECoG and fMRI category-selective signals in human ventral temporal cortex. Neuropsychologia 2016, 83:14-28. 10.1016/j.neuropsychologia.2015.07.024.
Jeffreys D.A. A face-responsive potential recorded from the human scalp. Exp. Brain Res. 1989, 78:193-202.
Jeffreys D.A. Evoked potential studies of face and object processing. Vis. Cogn. 1996, 3:1-38.
Jonas J., Maillard L., Frismand S., Colnat-Coulbois S., Vespignani H., Rossion B., Vignal J.-P. Self-face hallucination evoked by electrical stimulation of the human brain. Neurology 2014, 83:336-338. 10.1212/WNL.0000000000000628.
Jonas J., Rossion B., Brissart H., Frismand S., Jacques C., Hossu G., Colnat-Coulbois S., Vespignani H., Vignal J.-P., Maillard L. Beyond the core face-processing network: intracerebral stimulation of a face-selective area in the right anterior fusiform gyrus elicits transient prosopagnosia. Cortex 2015, 10.1016/j.cortex.2015.05.026.
Joyce C., Rossion B. The face-sensitive N170 and VPP components manifest the same brain processes: the effect of reference electrode site. Clin. Neurophysiol. 2005, 116:2613-2631.
Keil M.S., Cristobal G. Separating the chaff from the wheat: possible origins of the oblique effect. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2000, 17:697-710.
Kincade J.M. An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention. J. Neurosci. 2005, 25:4593-4604. 10.1523/JNEUROSCI.0236-05.2005.
Koessler L., Cecchin T., Colnat-Coulbois S., Vignal J.-P., Jonas J., Vespignani H., Ramantani G., Maillard L.G. Catching the invisible: mesial temporal source contribution to simultaneous EEG and SEEG recordings. Brain Topogr. 2014, 28:5-20. 10.1007/s10548-014-0417-z.
Kovacs G., Zimmer M., Banko E., Harza I., Antal A., Vidnyanszky Z. Electrophysiological correlates of visual adaptation to faces and body parts in humans. Cereb. Cortex 2006, 16:742-753.
Lewis M.B., Edmonds A.J. Face detection: mapping human performance. Perception 2003, 32:903-920.
Liu J., Harris A., Kanwisher N. Stages of processing in face perception: an MEG study. Nat. Neurosci. 2002, 5:910-916.
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. 2009, 62:281-290. 10.1016/j.neuron.2009.02.025.
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 oddball stimulation. Neuropsychologia 2014, 52:57-72. 10.1016/j.neuropsychologia.2013.10.022.
Liu-Shuang J., Torfs K., Rossion B. An objective electrophysiological marker of face individualisation impairment in acquired prosopagnosia with fast periodic visual stimulation. Neuropsychologia 2016, 83:100-113. 10.1016/j.neuropsychologia.2015.08.023.
McCarthy G., Wood C.C. Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr. Clin. Neurophysiol. Potentials Sect. 1985, 62:203-208. 10.1016/0168-5597(85)90015-2.
McCarthy G., Puce A., Belger A., Allison T. Electrophysiological studies of human face perception. II: response properties of face-specific potentials generated in occipitotemporal cortex. Cereb. Cortex 1999, 9:431-444.
McKeeff T.J., Remus D.A., Tong F. Temporal limitations in object processing across the human ventral visual pathway. J. Neurophysiol. 2007, 98:382-393.
Meeren H.K.M., de Gelder B., Ahlfors S.P., Hämäläinen M.S., Hadjikhani N. Different cortical dynamics in face and body perception: an MEG study. PLoS One 2013, 8:e71408. 10.1371/journal.pone.0071408.
Minnebusch D.A., Suchan B., Daum I. Losing your head: behavioral and electrophysiological effects of body inversion. J. Cogn. Neurosci. 2009, 21:865-874. 10.1162/jocn.2009.21074.
Nakamura K., Kawashima R., Sato N., Nakamura A., Sugiura M., Kato T., Hatano K., Ito K., Fukuda H., Schormann T., Zilles K. Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. Brain 2000, 123(Pt 9):1903-1912.
Nasr S., Echavarria C.E., Tootell R.B.H. Thinking outside the box: rectilinear shapes selectively activate scene-selective cortex. J. Neurosci. 2014, 34:6721-6735. 10.1523/JNEUROSCI.4802-13.2014.
Norcia A.M., Appelbaum L.G., Ales J.M., Cottereau B.R., Rossion B. The steady-state visual evoked potential in vision research: A review. J. Vis. 2015, 6(6):4. 10.1167/15.6.4.
Orlov T., Makin T.R., Zohary E. Topographic representation of the human body in the occipitotemporal cortex. Neuron 2010, 68:586-600. 10.1016/j.neuron.2010.09.032.
Peelen M.V., Downing P.E. Selectivity for the human body in the fusiform gyrus. J. Neurophysiol. 2005, 93:603-608. 10.1152/jn.00513.2004.
Potter M.C. Recognition and memory for briefly presented scenes. Front. Psychol. 2012, 3:1-9. 10.3389/fpsyg.2012.00032.
Potter M.C., Levy E.I. Recognition memory for a rapid sequence of pictures. J. Exp. Psychol. 1969, 81:10-15.
Puce A., Perrett D. Electrophysiology and brain imaging of biological motion. Philos. Trans. R. Soc. B Biol. Sci. 2003, 358:435-445. 10.1098/rstb.2002.1221.
Puce A., Allison T., Bentin S., Gore J.C., McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 1998, 18:2188-2199.
Regan D. Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine 1989, Elsevier, New York.
Rossion B., Jacques C. Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170. Neuroimage 2008, 39:1959-1979. 10.1016/j.neuroimage.2007.10.011.
Rossion B., Caharel S. ERP evidence for the speed of face categorization in the human brain: disentangling the contribution of low-level visual cues from face perception. Vis. Res. 2011, 51:1297-1311. 10.1016/j.visres.2011.04.003.
Rossion B., Jacques C. The N170: understanding the time-course of face perception in the human brain 2011, 115-142. The Oxford Handbook of ERP Components, New York. E.S. Kappenman, S.J. Luck (Eds.).
Rossion B., Gauthier I., Tarr M.J., Despland P., Bruyer R., Linotte S., Crommelinck M. The N170 occipito-temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face-specific processes in the human brain. Neuroreport 2000, 11:69-74.
Rossion B., Hanseeuw B., Dricot L. Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis. Brain Cogn. 2012, 79:138-157. 10.1016/j.bandc.2012.01.001.
Rossion B., Prieto E.A., 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 2012, 63:1585-1600. 10.1016/j.neuroimage.2012.08.033.
Rossion B., Jacques C., Liu-Shuang J. Fast periodic presentation of natural images reveals a robust face-selective electrophysiological response in the human brain. J. Vis. 2015, 15(1):1-18. (18). 10.1167/15.1.18.
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. 2003, 3:440-455. 10.1167/3.6.5.
Rousselet G.A., Husk J.S., Bennett P.J., Sekuler A.B. Time course and robustness of ERP object and face differences. J. Vis. 2008, 8(12):1-18. (3). 10.1167/8.12.3.
Schneider B.L., DeLong J.E., Busey T.A. Added noise affects the neural correlates of upright and inverted faces differently. J. Vis. 2007, 7(4):1-24. (4). 10.1167/7.4.4.
Schwarzlose R.F., Baker C.I., Kanwisher N. Separate face and body selectivity on the fusiform gyrus. J. Neurosci. 2005, 25:11055-11059. 10.1523/JNEUROSCI.2621-05.2005.
Sergent J., Ohta S., Macdonald B. Functional neuroanatomy of face and object processing - a positron emission tomography study. Brain 1992, 115:15-36.
Srinivasan R., Russell D.P., Edelman G.M., Tononi G. Increased synchronization of neuromagnetic responses during conscious perception. J. Neurosci. 1999, 19:5435-5448.
Tanskanen T., Nasanen R., Montez T., Paallysaho J., Hari R. Face recognition and cortical responses show similar sensitivity to noise spatial frequency. Cereb. Cortex 2005, 15:526-534.
Taylor J.C., Roberts M.V., Downing P.E., Thierry G. Functional characterisation of the extrastriate body area based on the N1 ERP component. Brain Cogn. 2010, 73:153-159. 10.1016/j.bandc.2010.04.001.
Thierry G., Pegna A.J., Dodds C., Roberts M., Basan S., Downing P. An event-related potential component sensitive to images of the human body. NeuroImage 2006, 32:871-879. 10.1016/j.neuroimage.2006.03.060.
Thompson J.C., Clarke M., Stewart T., Puce A. Configural processing of biological motion in human superior temporal sulcus. J. Neurosci. 2005, 25:9059-9066. 10.1523/JNEUROSCI.2129-05.2005.
Tsao D.Y., Moeller S., Freiwald W.A. Comparing face patch systems in macaques and humans. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19514-19519. 10.1073/pnas.0809662105.
Weiner K.S., Grill-Spector K. Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. NeuroImage 2010, 52:1559-1573. 10.1016/j.neuroimage.2010.04.262.
Weiner K.S., Grill-Spector K. Not one extrastriate body area: using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex. NeuroImage 2011, 56:2183-2199. 10.1016/j.neuroimage.2011.03.041.
Zhen Z., Yang Z., Huang L., Kong X., Wang X., Dang X., Huang Y., Song Y., Liu J. Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. Neuroimage 2015, 113:13-25. 10.1016/j.neuroimage.2015.03.010.