Intracerebral electrical stimulation of a face-selective area in the right inferior occipital cortex impairs individual face discrimination Jacques Jonas a,b,c,d,e, ⁎, Bruno Rossion e , Julien Krieg b,c , Laurent Koessler b,c , Sophie Colnat-Coulbois d,f , Hervé Vespignani a,b,c,d , Corentin Jacques e , Jean-Pierre Vignal a,b,c , Hélène Brissart a , Louis Maillard a,b,c,d a Service de Neurologie, Centre Hospitalier Universitaire de Nancy, 29 Avenue du Maréchal de Lattre de Tassigny, 54000 Nancy, France b Université de Lorraine, CRAN, UMR 7039, Campus Sciences, Boulevard des Aiguillettes, 54500 Vandœuvre-lès-Nancy, France c CNRS, CRAN, UMR 7039, Campus Sciences, Boulevard des Aiguillettes, 54500 Vandœuvre-lès-Nancy, France d Faculté de Médecine de Nancy, Université de Lorraine, 9 Avenue de la Forêt de Haye, 54500 Vandœuvre-lès-Nancy, France e Université Catholique de Louvain, 10 Place du Cardinal Mercier, 1348 Louvain-La-Neuve, Belgium f Service de Neurochirurgie, Centre Hospitalier Universitaire de Nancy, 29 Avenue du Maréchal de Lattre de Tassigny, 54000 Nancy, France abstract article info Article history: Accepted 6 June 2014 Available online 14 June 2014 Keywords: Intracerebral recordings Individual face discrimination Repetition suppression Electrical brain stimulation Occipital face area Fast periodic visual stimulation During intracerebral stimulation of the right inferior occipital cortex, a patient with refractory epilepsy was tran- siently impaired at discriminating two simultaneously presented photographs of unfamiliar faces. The critical electrode contact was located in the most posterior face-selective brain area of the human brain (right “occipital face area”, rOFA) as shown both by low- (ERP) and high-frequency (gamma) electrophysiological responses as well as a face localizer in fMRI. At this electrode contact, periodic visual presentation of 6 different faces by second evoked a larger electrophysiological periodic response at 6 Hz than when the same face identity was repeated at the same rate. This intracerebral EEG repetition suppression effect was markedly reduced when face stimuli were presented upside-down, a manipulation that impairs individual face discrimination. These findings provide orig- inal evidence for a causal relationship between the face-selective right inferior occipital cortex and individual face discrimination, independently of long-term memory representations. More generally, they support the function- al value of electrophysiological repetition suppression effects, indicating that these effects can be used as an index of a necessary neural representation of the changing stimulus property. © 2014 Elsevier Inc. All rights reserved. Introduction One of the most impressive functions of the human brain is its ability to differentiate complex visual forms (DiCarlo and Cox, 2007). The human face constitutes the most familiar, socially relevant, and complex visual form, so that discriminating individual faces requires elaborate and refined perceptual skills called for by few other categories of ob- jects. Despite the high similarity among faces and their complex config- uration of several parts (eyes, nose, mouth, etc.), adults attain a high degree of proficiency with these skills. Yet, to date, the neural basis of in- dividual face discrimination in the human brain remains by and large a mystery. In humans, there is a large bilateral network of occipito-temporal areas responding preferentially to faces (i.e., face-selective areas), with right hemispheric dominance (e.g., Allison et al., 1994; Calder and Young, 2005; Haxby et al., 2000; Rossion et al., 2012a; Sergent et al., 1992; Weiner and Grill-Spector, 2010). To investigate sensitivity to individual faces of these areas, functional magnetic resonance imaging (fMRI) studies have taken advantage of the reduction of neural activity following repetition of the same stimulus (repetition suppression, also referred to fMR-adaptation or habituation; Grill-Spector and Malach, 2001; Grill-Spector et al., 2006). The rationale of this approach is that populations of neurons sensitive to differences between individual faces show a smaller response when the same face identity is repeated compared to the presentation of different face identities. Many fMRI studies have reported such decreases to individual face repetition in face-selective areas of the ventral occipito-temporal cortex (e.g., Gauthier et al., 2000; Grill-Spector and Malach, 2001; Andrews and Ewbank, 2004; Schiltz et al., 2006; Gilaie-Dotan and Malach, 2007; Davies-Thompson et al., 2009; Xu and Biederman, 2010; Ewbank et al., 2013). Multivariate pattern analyses of fMRI data have also iden- tified various clusters of voxels in the ventral occipito-temporal cortex that are sensitive to individual faces (Goesaert and Op de Beeck, 2013; Kriegeskorte et al., 2007; Nestor et al., 2011). Taken together, the obser- vations of these studies point to a distributed representation of individ- ual face information in the ventral occipito-temporal cortex, with a right hemispheric advantage. However, the relationship between these ef- fects – in particular the face identity repetition suppression effects in neuroimaging – and behavioral performance at individual face NeuroImage 99 (2014) 487–497 ⁎ Corresponding author at: Service de Neurologie, Hôpital Central, Centre Hospitalier Universitaire de Nancy, 29 Avenue du Maréchal de Lattre de Tassigny, 54000 Nancy, France. E-mail address: j.jonas@chu-nancy.fr (J. Jonas). http://dx.doi.org/10.1016/j.neuroimage.2014.06.017 1053-8119/© 2014 Elsevier Inc. All rights reserved. Contents lists available at ScienceDirect NeuroImage journal homepage: www.elsevier.com/locate/ynimg