Brain Topography

, Volume 31, Issue 6, pp 972–984 | Cite as

Increased Early Sensitivity to Eyes in Mouthless Faces: In Support of the LIFTED Model of Early Face Processing

  • Roxane J. ItierEmail author
  • Frank Preston
Original Paper


The N170 ERP component is a central neural marker of early face perception usually thought to reflect holistic processing. However, it is also highly sensitive to eyes presented in isolation and to fixation on the eyes within a full face. The lateral inhibition face template and eye detector (LIFTED) model (Nemrodov et al. in NeuroImage 97:81–94, 2014) integrates these views by proposing a neural inhibition mechanism that perceptually glues features into a whole, in parallel to the activity of an eye detector that accounts for the eye sensitivity. The LIFTED model was derived from a large number of results obtained with intact and eyeless faces presented upright and inverted. The present study provided a control condition to the original design by replacing eyeless with mouthless faces, hereby enabling testing of specific predictions derived from the model. Using the same gaze-contingent approach, we replicated the N170 eye sensitivity regardless of face orientation. Furthermore, when eyes were fixated in upright faces, the N170 was larger for mouthless compared to intact faces, while inverted mouthless faces elicited smaller amplitude than intact inverted faces when fixation was on the mouth and nose. The results are largely in line with the LIFTED model, in particular with the idea of an inhibition mechanism involved in holistic processing of upright faces and the lack of such inhibition in processing inverted faces. Some modifications to the original model are also proposed based on these results.


Faces Eyes N170 ERPs Gaze-contingent procedure Inhibition 



This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grants #418431); the Ontario government (Early Researcher Award, ER11-08-172); the Canada Foundation for Innovation (Grant #213322); and the Canada Research Chairs program (Grants #213322 and #230407) to RJI. We would also like to thank Marina Ren for help with testing, supported by an NSERC Undergraduate Studies Research Award (USRA).

Supplementary material

10548_2018_663_MOESM1_ESM.docx (293 kb)
Supplementary material 1 (DOCX 292 KB)


  1. Allison T, Puce A, McCarthy G (2002) Category-sensitive excitatory and inhibitory processes in human extrastriate cortex. J Neurophysiol 88(5):2864–2868CrossRefPubMedGoogle Scholar
  2. Bentin S, Allison T, Puce A, Perez E, McCarthy G (1996) Electrophysiological studies of face perception in humans. J Cogn Neurosci 8:551–565CrossRefPubMedPubMedCentralGoogle Scholar
  3. de Haan M, Pascalis O, Johnson MH (2002) Specialization of neural mechanisms underlying face recognition in human infants. J Cogn Neurosci 14(2):1–11CrossRefGoogle Scholar
  4. de Lissa P, McArthur G, Hawelka S, Palermo R, Mahajan Y, Hutzler F (2014) Fixation location on upright and inverted faces modulates the N170. Neuropsychologia 57, 1–11CrossRefPubMedGoogle Scholar
  5. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21CrossRefPubMedGoogle Scholar
  6. Eimer M (1998) Does the face-specific N170 component reflect the activity of a specialized eye processor? Neuroreport 9(1399019440):2945–2948CrossRefPubMedGoogle Scholar
  7. Eimer M (2000a) Effects of face inversion on the structural encoding and recognition of faces. Evidence from event-related brain potentials. Brain Res Cogn Brain Res 10(1–2):145–158CrossRefPubMedGoogle Scholar
  8. Eimer M (2000b) The face-specific N170 component reflects late stages in the structural encoding of faces. Neuroreport 11(10):2319–2324CrossRefPubMedGoogle Scholar
  9. Eimer M (2011) The face-sensitive N170 component of the event-related brain potential. In: Calder AJ, Rhodes G, Johnson MH and Haxby JV (eds) The oxford handbook of face perception. Oxford University Press, Oxford, pp. 329–344Google Scholar
  10. Engell AD, McCarthy G (2014) Face, eye, and body selective responses in fusiform gyrus and adjacent cortex: an intracranial EEG study. Front Hum Neurosci 8:642CrossRefPubMedPubMedCentralGoogle Scholar
  11. Freiwald WA, Tsao DY, Livingstone MS (2009) A face feature space in the macaque temporal lobe. Nat Neurosci 12(9):1187–1196CrossRefPubMedPubMedCentralGoogle Scholar
  12. George N, Evans J, Fiori N, Davidoff J, Renault B (1996) Brain events related to normal and moderetately scrambled faces. Brain Res Cogn Brain Res 4(2):65–76CrossRefPubMedGoogle Scholar
  13. Itier RJ, Neath-Tavares KN (2017) Effects of task demands on the early neural processing of fearful and happy facial expressions. Brain Res 1663:38–50CrossRefPubMedPubMedCentralGoogle Scholar
  14. Itier RJ, Taylor MJ (2002) Inversion and contrast polarity reversal affect both encoding and recognition processes of unfamiliar faces: a repetition study using ERPs. NeuroImage 15(2):353–372CrossRefPubMedGoogle Scholar
  15. Itier RJ, Latinus M, Taylor MJ (2006) Face, eye and object early processing: what is the face specificity? NeuroImage 29(2):667–676CrossRefPubMedGoogle Scholar
  16. Itier RJ, Alain C, Sedore K, McIntosh AR (2007) Early face processing specificity: it’s in the eyes! J Cogn Neurosci 19(11):1815–1826CrossRefPubMedGoogle Scholar
  17. Itier RJ, Van Roon P, Alain C (2011) Species sensitivity of early face eye processing NeuroImage 54(1):705–713CrossRefPubMedGoogle Scholar
  18. 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(6):8, 1–16CrossRefGoogle Scholar
  19. Kloth N, Itier RJ, Schweinberger SR (2013) Combined effects of inversion and feature removal on N170 responses elicited by faces and car fronts. Brain Cogn 81(3):321–328CrossRefPubMedPubMedCentralGoogle Scholar
  20. Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. Trends Cogn Sci 6(6):255–260CrossRefPubMedGoogle Scholar
  21. McPartland J, Cheung CH, Perszyk D, Mayes LC (2010) Face-related ERPs are modulated by point of gaze. Neuropsychologia 48(12):3657–3660CrossRefPubMedPubMedCentralGoogle Scholar
  22. Neath KN, Itier RJ (2015) Fixation to features and neural processing of facial expressions in a gender discrimination task. Brain Cogn 99:97–111CrossRefPubMedPubMedCentralGoogle Scholar
  23. Neath-Tavares KN, Itier RJ (2016) Neural processing of fearful and happy facial expressions during emotion-relevant and emotion-irrelevant tasks: a fixation-to-feature approach. Biol Psychol 119:122–140CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nemrodov D, Itier RJ (2011) The role of eyes in early face processing: a rapid adaptation study of the inversion effect. Br J Psychol 102(4):783–798CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nemrodov D, Anderson T, Preston FF, Itier RJ (2014) Early sensitivity for eyes within faces: a new neuronal account of holistic and featural processing. NeuroImage 97, 81–94CrossRefPubMedPubMedCentralGoogle Scholar
  26. Rossion B (2009) Distinguishing the cause and consequence of face inversion: the perceptual field hypothesis. Acta Physiol 132(3):300–312Google Scholar
  27. Rossion B, Jacques C (2012) The N170: understanding the time course of face perception in the human brain. In: Luck SJ, and Kappenman ES (eds) The oxford handbook of event-related potential components. Oxford university Press, Oxford, pp. 115–141Google Scholar
  28. Rossion B, Taubert J (2017) Commentary: the code for facial identity in the primate brain. Front Hum Neurosci 2017 11:550CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rossion B, Delvenne JF, Debatisse D, Goffaux V, Bruyer R, Crommelinck M et al (1999) Spatio-temporal localization of the face inversion effect: an event-related potentials study. Biol Psychol 50(399388900):173–189CrossRefPubMedGoogle Scholar
  30. Rossion B, Gauthier I, Tarr MJ, Despland P, Bruyer R, Linotte S et al (2000) 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 11(120147456):69–74CrossRefPubMedGoogle Scholar
  31. Rousselet GA, Ince RA, van Rijsbergen NJ, Schyns PG (2014) Eye coding mechanisms in early human face event-related potentials. J Vis 14(13):1–24CrossRefGoogle Scholar
  32. Sadeh B, Yovel G (2010) Why is the N170 enhanced for inverted faces? An ERP competition experiment. NeuroImage 53(2), 782–789CrossRefPubMedGoogle Scholar
  33. Sagiv N, Bentin S (2001) Structural encoding of human and schematic faces: holistic and part-based processes. J Cogn Neurosci 13(7):937–951CrossRefGoogle Scholar
  34. Schyns PG, Jentzsch I, Johnson M, Schweinberger SR, Gosselin F (2003) A principled method for determining the functionality of brain responses. Neuroreport 14:1665–1669CrossRefPubMedGoogle Scholar
  35. Shepherd J, Davies G, Ellis H (1981) Studies of cue saliency. In: Davies G, Ellis HD, Shepherd J (eds) Perceiving and remembering faces. Academic Press, New York, pp 105–131Google Scholar
  36. Tanaka JW, Gordon I (2011) Features, configuration, and holistic face processing. In: Calder AJ, Rhodes G, Johnson MJ, Haxby JV (eds) The Oxford handbook of face perception. Oxford University Press, New York, pp 177–194Google Scholar
  37. Taylor MJ, Edmonds GE, McCarthy G, Allison T (2001) Eyes first! eye processing develops before face processing in children. Neuroreport 12(8):1671–1676CrossRefPubMedGoogle Scholar
  38. Wang Y, Fujita I, Murayama Y (2000) Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nat Neurosci 3(8):807–813CrossRefPubMedGoogle Scholar
  39. Wiese H, Stahl J, Schweinberger SR (2009) Configural processing of other-race faces is delayed but not decreased. Biol Psychol 81(2):103–109CrossRefPubMedGoogle Scholar
  40. Zerouali Y, Lina JM, Jemel B (2013) Optimal eye-gaze fixation position for face-related neural responses. PloS ONE 8(6):e60128CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of WaterlooWaterlooCanada

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