Brain Structure and Function

, Volume 222, Issue 9, pp 4271–4282 | Cite as

The occipital face area is causally involved in the formation of identity-specific face representations

  • Géza Gergely AmbrusEmail author
  • Maria Dotzer
  • Stefan R. Schweinberger
  • Gyula Kovács
Original Article


Transcranial magnetic stimulation (TMS) and neuroimaging studies suggest a role of the right occipital face area (rOFA) in early facial feature processing. However, the degree to which rOFA is necessary for the encoding of facial identity has been less clear. Here we used a state-dependent TMS paradigm, where stimulation preferentially facilitates attributes encoded by less active neural populations, to investigate the role of the rOFA in face perception and specifically in image-independent identity processing. Participants performed a familiarity decision task for famous and unknown target faces, preceded by brief (200 ms) or longer (3500 ms) exposures to primes which were either an image of a different identity (DiffID), another image of the same identity (SameID), the same image (SameIMG), or a Fourier-randomized noise pattern (NOISE) while either the rOFA or the vertex as control was stimulated by single-pulse TMS. Strikingly, TMS to the rOFA eliminated the advantage of SameID over DiffID condition, thereby disrupting identity-specific priming, while leaving image-specific priming (better performance for SameIMG vs. SameID) unaffected. Our results suggest that the role of rOFA is not limited to low-level feature processing, and emphasize its role in image-independent facial identity processing and the formation of identity-specific memory traces.


Face perception Identity Occipital face area Priming Transcranial magnetic stimulation 



This work was supported by a Deutsche Forschungsgemeinschaft Grant (Grant Number KO 3918/1-2; 2-2 and 5-1). The authors would like to thank Catarina Amado, Anna-Barbara C. Trimborn, and Fabienne Windel for their assistance in participant recruitment and data collection.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.


This work was supported by a Deutsche Forschungsgemeinschaft Grant (Grant Number KO 3918/1-2; 2-2 and 5-1).


  1. Amado C, Hermann P, Kovács P et al (2016) The contribution of surprise to the prediction based modulation of fMRI responses. Neuropsychologia 84:105–112. doi: 10.1016/j.neuropsychologia.2016.02.003 CrossRefPubMedGoogle Scholar
  2. Barron HC, Garvert MM, Behrens TEJ (2016) Repetition suppression: a means to index neural representations using BOLD? Philos Trans R Soc Lond B Biol Sci 371:51–56. doi: 10.1098/rstb.2015.0355 CrossRefGoogle Scholar
  3. Bona S, Cattaneo Z, Silvanto J (2016) Investigating the causal role of rOFA in holistic detection of mooney faces and objects: an fMRI-guided TMS study. Brain Stimul 9:594–600CrossRefPubMedGoogle Scholar
  4. Bouvier SE, Engel SA (2006) Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb Cortex 16:183–191. doi: 10.1093/cercor/bhi096 CrossRefPubMedGoogle Scholar
  5. Bruce V, Valentine T (1985) Identity priming in the recognition of familiar faces. Br J Psychol 76:373–383. doi: 10.1111/j.2044-8295.1985.tb01960.x CrossRefPubMedGoogle Scholar
  6. Campana G, Cowey A, Walsh V (2002) Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb Cortex 12:663–669. doi: 10.1093/cercor/12.6.663 CrossRefPubMedGoogle Scholar
  7. Cattaneo L (2010) Tuning of ventral premotor cortex neurons to distinct observed grasp types: a TMS-priming study. Exp Brain Res 207:165–172. doi: 10.1007/s00221-010-2454-5 CrossRefPubMedGoogle Scholar
  8. Cattaneo Z, Silvanto J (2008a) Investigating visual motion perception using the transcranial magnetic stimulation-adaptation paradigm. NeuroReport 19:1423–1427. doi: 10.1097/WNR.0b013e32830e0025 CrossRefPubMedGoogle Scholar
  9. Cattaneo Z, Silvanto J (2008b) Time course of the state-dependent effect of transcranial magnetic stimulation in the TMS-adaptation paradigm. Neurosci Lett 443:82–85. doi: 10.1016/j.neulet.2008.07.051 CrossRefPubMedGoogle Scholar
  10. Cattaneo Z, Rota F, Vecchi T, Silvanto J (2008) Using state-dependency of transcranial magnetic stimulation (TMS) to investigate letter selectivity in the left posterior parietal cortex: a comparison of TMS-priming and TMS-adaptation paradigms. Eur J Neurosci 28:1924–1929. doi: 10.1111/j.1460-9568.2008.06466.x CrossRefPubMedGoogle Scholar
  11. Cattaneo Z, Rota F, Walsh V et al (2009) TMS-adaptation reveals abstract letter selectivity in the left posterior parietal cortex. Cereb Cortex 19:2321–2325. doi: 10.1093/cercor/bhn249 CrossRefPubMedGoogle Scholar
  12. Cattaneo Z, Devlin JT, Salvini F et al (2010) The causal role of category-specific neuronal representations in the left ventral premotor cortex (PMv) in semantic processing. Neuroimage 49:2728–2734. doi: 10.1016/j.neuroimage.2009.10.048 CrossRefPubMedGoogle Scholar
  13. Cattaneo Z, Bona S, Silvanto J (2012) Cross-adaptation combined with TMS reveals a functional overlap between vision and imagery in the early visual cortex. Neuroimage 59:3015–3020. doi: 10.1016/j.neuroimage.2011.10.022 CrossRefPubMedGoogle Scholar
  14. Cziraki C, Greenlee MW, Kovács G (2010) Neural correlates of high-level adaptation-related after effects. J Neurophysiol 103:1410–1417CrossRefPubMedGoogle Scholar
  15. Davies-Thompson J, Andrews TJ (2012) Intra- and inter-hemispheric connectivity between face-selective regions in the human brain. J Neurophysiol. doi: 10.1152/jn.01171.2011 PubMedPubMedCentralGoogle Scholar
  16. Delvenne JF, Seron X, Coyette F, Rossion B (2004) Evidence for perceptual deficits in associative visual (prosop)agnosia: a single-case study. Neuropsychologia 42:597–612. doi: 10.1016/j.neuropsychologia.2003.10.008 CrossRefPubMedGoogle Scholar
  17. Dricot L, Sorger B, Schiltz C et al (2008) The roles of “face” and “non-face” areas during individual face perception: evidence by fMRI adaptation in a brain-damaged prosopagnosic patient. Neuroimage 40:318–332. doi: 10.1016/j.neuroimage.2007.11.012 CrossRefPubMedGoogle Scholar
  18. Duchaine B, Yovel G (2015) A revised neural framework for face processing. Annu Rev Vis Sci 1:393–416. doi: 10.1146/annurev-vision-082114-035518 CrossRefPubMedGoogle Scholar
  19. Duecker F, Sack AT (2013) Pre-stimulus sham TMS facilitates target detection. PLoS One. doi: 10.1371/journal.pone.0057765 Google Scholar
  20. Duecker F, de Graaf TA, Jacobs C, Sack AT (2013) Time- and task-dependent non-neural effects of real and sham TMS. PLoS One. doi: 10.1371/journal.pone.0073813 Google Scholar
  21. Ellis AW, Young AW, Flude BM, Hay DC (1987) Repetition priming of face recognition. Q J Exp Psychol Sect A 39:193–210. doi: 10.1080/14640748708401784 CrossRefGoogle Scholar
  22. Ewbank MP, Henson RN, Rowe JB et al (2013) Different neural mechanisms within occipitotemporal cortex underlie repetition suppression across same and different-size faces. Cereb Cortex 23:1073–1084. doi: 10.1093/cercor/bhs070 CrossRefPubMedGoogle Scholar
  23. Frässle S, Paulus FM, Krach S et al (2016) Mechanisms of hemispheric lateralization: asymmetric interhemispheric recruitment in the face perception network. Neuroimage 124:977–988. doi: 10.1016/j.neuroimage.2015.09.055 CrossRefPubMedGoogle Scholar
  24. Gilaie-Dotan S, Silvanto J, Schwarzkopf DS, Rees G (2010) Investigating representations of facial identity in human ventral visual cortex with transcranial magnetic stimulation. Front Hum Neurosci 4:50PubMedPubMedCentralGoogle Scholar
  25. Grill-Spector K, Henson RN, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10:14–23. doi: 10.1016/j.tics.2005.11.006 CrossRefPubMedGoogle Scholar
  26. Gschwind M, Pourtois G, Schwartz S et al (2012) White-matter connectivity between face-responsive regions in the human brain. Cereb Cortex 22:1564–1576. doi: 10.1093/cercor/bhr226 CrossRefPubMedGoogle Scholar
  27. Guntupalli JS, Wheeler KG, Gobbini MI (2017) Disentangling the representation of identity from head view along the human face processing pathway. Cereb Cortex 27(1):46–53CrossRefPubMedGoogle Scholar
  28. Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223–233. doi: 10.1016/S1364-6613(00)01482-0 CrossRefPubMedGoogle Scholar
  29. Jacobs C, de Graaf TA, Goebel R, Sack AT (2012) The temporal dynamics of early visual cortex involvement in behavioral priming. PLoS One 7:e48808. doi: 10.1371/journal.pone.0048808 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jacoby LL, Woloshyn V, Kelley C (1989) Becoming famous without being recognized: unconscious influences of memory produced by dividing attention. J Exp Psychol Gen 118:115–125. doi: 10.1037/0096-3445.118.2.115 CrossRefGoogle Scholar
  31. Jonas J, Descoins M, Koessler L et al (2012) Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia. Neuroscience 222:281–288. doi: 10.1016/j.neuroscience.2012.07.021 CrossRefPubMedGoogle Scholar
  32. Jonas J, Rossion B, Krieg J et al (2014) Intracerebral electrical stimulation of a face-selective area in the right inferior occipital cortex impairs individual face discrimination. Neuroimage 99:487–497. doi: 10.1016/j.neuroimage.2014.06.017 CrossRefPubMedGoogle Scholar
  33. Kadosh KC, Walsh V, Kadosh RC (2011) Investigating face-property specific processing in the right OFA. Soc Cogn Affect Neurosci 6:58–65. doi: 10.1093/scan/nsq015 CrossRefPubMedGoogle Scholar
  34. Kaiser D, Walther C, Schweinberger SR, Kovács G (2013) Dissociating the neural bases of repetition-priming and adaptation in the human brain for faces. J Neurophysiol 110:2727–2738. doi: 10.1152/jn.00277.2013 CrossRefPubMedGoogle Scholar
  35. Kar K, Krekelberg B (2016) Testing the assumptions underlying fMRI adaptation using intracortical recordings in area MT. Cortex 80:21–34. doi: 10.1016/j.cortex.2015.12.011 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kohn A (2007) Visual adaptation: physiology, mechanisms, and functional benefits. J Neurophysiol 97:3155–3164. doi: 10.1152/jn.00086.2007 CrossRefPubMedGoogle Scholar
  37. Kovács G, Schweinberger SR (2016) Repetition suppression—an integrative view. Cortex 80:1–4CrossRefPubMedGoogle Scholar
  38. Landau JD, Leed SA (2012) The illusion of fame: how the nonfamous become famous. Am J Psychol 125:351–360. doi: 10.5406/amerjpsyc.125.3.0351 CrossRefPubMedGoogle Scholar
  39. Mattavelli G, Cattaneo Z, Papagno C (2011) Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task. Neuropsychologia 49:992–998. doi: 10.1016/j.neuropsychologia.2011.01.038 CrossRefPubMedGoogle Scholar
  40. Perini F, Cattaneo L, Carrasco M, Schwarzbach J (2012) Occipital transcranial magnetic stimulation has an activity-dependent suppressive effect. J Neurosci 32:12361–12365. doi: 10.1523/JNEUROSCI.5864-11.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pitcher D, Walsh V, Yovel G, Duchaine B (2007) TMS evidence for the involvement of the right occipital face area in early face processing. Curr Biol 17:1568–1573CrossRefPubMedGoogle Scholar
  42. Pitcher D, Garrido L, Walsh V, Duchaine BC (2008) Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. J Neurosci 28:8929–8933. doi: 10.1523/JNEUROSCI.1450-08.2008 CrossRefPubMedGoogle Scholar
  43. Pitcher D, Goldhaber T, Duchaine B et al (2012) Two critical and functionally distinct stages of face and body perception. J Neurosci 32:15877–15885. doi: 10.1523/JNEUROSCI.2624-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pyles JA, Verstynen TD, Schneider W, Tarr MJ (2013) Explicating the face perception network with white matter connectivity. PLoS One. doi: 10.1371/journal.pone.0061611 Google Scholar
  45. Rajimehr R, Young JC, Tootell RBH (2009) An anterior temporal face patch in human cortex, predicted by macaque maps. Proc Natl Acad Sci USA 106:1995–2000. doi: 10.1073/pnas.0807304106 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Renzi C, Vecchi T, Silvanto J, Cattaneo Z (2011) Overlapping representations of numerical magnitude and motion direction in the posterior parietal cortex: a TMS-adaptation study. Neurosci Lett 490:145–149. doi: 10.1016/j.neulet.2010.12.045 CrossRefPubMedGoogle Scholar
  47. Rossion B (2008) Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. Neuroimage 40:423–426CrossRefPubMedGoogle Scholar
  48. Rossion B (2014) Understanding face perception by means of prosopagnosia and neuroimaging. Front Biosci Elit 6E:258–307CrossRefGoogle Scholar
  49. Rossion B, Caldara R, Seghier M et al (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126:2381–2395. doi: 10.1093/brain/awg241 CrossRefPubMedGoogle Scholar
  50. Rotshtein P, Henson RN, Treves A et al (2005) Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat Neurosci 8:107–113. doi: 10.1038/nn1370 CrossRefPubMedGoogle Scholar
  51. Schiltz C, Rossion B (2006) Faces are represented holistically in the human occipito-temporal cortex. Neuroimage 32:1385–1394. doi: 10.1016/j.neuroimage.2006.05.037 CrossRefPubMedGoogle Scholar
  52. Schweinberger SR, Pickering EC, Burton AM, Kaufmann JM (2002a) Human brain potential correlates of repetition priming in face and name recognition. Neuropsychologia 40:2057–2073. doi: 10.1016/S0028-3932(02)00050-7 CrossRefPubMedGoogle Scholar
  53. Schweinberger SR, Pickering EC, Jentzsch I et al (2002b) Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions. Cogn Brain Res 14:398–409. doi: 10.1016/S0926-6410(02)00142-8 CrossRefGoogle Scholar
  54. Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21:1–10CrossRefPubMedPubMedCentralGoogle Scholar
  55. Silvanto J, Muggleton NG, Cowey A, Walsh V (2007) Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur J Neurosci 25:1874–1881. doi: 10.1111/j.1460-9568.2007.05440.x CrossRefPubMedGoogle Scholar
  56. Silvanto J, Cattaneo Z, Battelli L, Pascual-Leone A (2008a) Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. J Neurophysiol 99:2725–2730. doi: 10.1152/jn.01392.2007 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Silvanto J, Muggleton N, Walsh V (2008b) State-dependency in brain stimulation studies of perception and cognition. Trends Cogn Sci 12:447–454CrossRefPubMedGoogle Scholar
  58. Solomon-Harris LM, Mullin CR, Steeves JKE (2013) TMS to the “occipital face area” affects recognition but not categorization of faces. Brain Cogn 83:245–251CrossRefPubMedGoogle Scholar
  59. Sorger B, Goebel R, Schiltz C, Rossion B (2007) Understanding the functional neuroanatomy of acquired prosopagnosia. Neuroimage 35:836–852. doi: 10.1016/j.neuroimage.2006.09.051 CrossRefPubMedGoogle Scholar
  60. Steeves JKE, Culham JC, Duchaine BC et al (2006) The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 44:594–609CrossRefPubMedGoogle Scholar
  61. Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci USA 105:19514–19519. doi: 10.1073/pnas.0809662105 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Vogels R (2016) Sources of adaptation of inferior temporal cortical responses. Cortex 80:185–195CrossRefPubMedGoogle Scholar
  63. Walther C, Schweinberger SR, Kaiser D, Kovács G (2013) Neural correlates of priming and adaptation in familiar face perception. Cortex 49:1963–1977. doi: 10.1016/j.cortex.2012.08.012 CrossRefPubMedGoogle Scholar
  64. Willenbockel V, Sadr J, Fiset D et al (2010) Controlling low-level image properties: the SHINE toolbox. Behav Res Methods 42:671–684. doi: 10.3758/brm.42.3.671 CrossRefPubMedGoogle Scholar
  65. Yang H, Susilo T, Duchaine B (2016) The anterior temporal face area contains invariant representations of face identity that can persist despite the loss of right FFA and OFA. Cereb Cortex 26:1096–1107. doi: 10.1093/cercor/bhu289 CrossRefPubMedGoogle Scholar
  66. Zimmer M, Zbant A, Németh K et al (2015) Adaptation duration dissociates category-, image-, and person-specific processes on face-evoked event-related potentials. Front Psychol 6:1–13. doi: 10.3389/fpsyg.2015.01945 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institute of PsychologyFriedrich Schiller University JenaJenaGermany
  2. 2.DFG Research Unit Person PerceptionFriedrich Schiller University JenaJenaGermany
  3. 3.Brain Imaging Centre, Research Centre for Natural SciencesHungarian Academy of SciencesBudapestHungary

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