Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Image credits: DiffID: By Fortepan/Kotnyek Antal [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0)], via Wikimedia Commons. (Hédi Váradi, Hungarian actress). SameID: Armin Linnartz (CC BY-SA 3.0 de), via Wikimedia Commons. SameIMG: By OfficevonStetten (Public domain or CC BY-SA 3.0), via Wikimedia Commons (Angela Merkel, the current German Chancellor). These images were not a part of the actual stimulus set
Similar content being viewed by others
References
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
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
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 9:594–600
Bouvier SE, Engel SA (2006) Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb Cortex 16:183–191. doi:10.1093/cercor/bhi096
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
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
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
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
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
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
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
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
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
Cziraki C, Greenlee MW, Kovács G (2010) Neural correlates of high-level adaptation-related after effects. J Neurophysiol 103:1410–1417
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
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
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
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
Duecker F, Sack AT (2013) Pre-stimulus sham TMS facilitates target detection. PLoS One. doi:10.1371/journal.pone.0057765
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
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
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
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
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 4:50
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
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
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):46–53
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
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
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
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
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
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
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
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
Kohn A (2007) Visual adaptation: physiology, mechanisms, and functional benefits. J Neurophysiol 97:3155–3164. doi:10.1152/jn.00086.2007
Kovács G, Schweinberger SR (2016) Repetition suppression—an integrative view. Cortex 80:1–4
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
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
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
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 17:1568–1573
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
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
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
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
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
Rossion B (2008) Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. Neuroimage 40:423–426
Rossion B (2014) Understanding face perception by means of prosopagnosia and neuroimaging. Front Biosci Elit 6E:258–307
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
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
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
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
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
Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21:1–10
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
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
Silvanto J, Muggleton N, Walsh V (2008b) State-dependency in brain stimulation studies of perception and cognition. Trends Cogn Sci 12:447–454
Solomon-Harris LM, Mullin CR, Steeves JKE (2013) TMS to the “occipital face area” affects recognition but not categorization of faces. Brain Cogn 83:245–251
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
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 44:594–609
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
Vogels R (2016) Sources of adaptation of inferior temporal cortical responses. Cortex 80:185–195
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
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
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
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
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Funding
This work was supported by a Deutsche Forschungsgemeinschaft Grant (Grant Number KO 3918/1-2; 2-2 and 5-1).
Rights and permissions
About this article
Cite this article
Ambrus, G.G., Dotzer, M., Schweinberger, S.R. et al. The occipital face area is causally involved in the formation of identity-specific face representations. Brain Struct Funct 222, 4271–4282 (2017). https://doi.org/10.1007/s00429-017-1467-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-017-1467-2