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International audience; Despite being of primary importance for fundamental research and clinical studies, the relationship between local neural population activity and scalp electroencephalography (EEG) in humans remains largely unknown. Here we report simultaneous scalp and intracerebral EEG responses to face stimuli in a unique epileptic patient implanted with 27 intracerebral recording contacts in the right occipitotemporal cortex. The patient was shown images of faces appearing at a frequency of 6 Hz, which elicits neural responses at this exact frequency. Response quantification at this frequency allowed to objectively relate the neural activity measured inside and outside the brain. The patient exhibited typical 6 Hz responses on the scalp at the right occipitotemporal sites. Moreover, there was a clear spatial correspondence between these scalp responses and intracerebral signals in the right lateral inferior occipital gyrus, both in amplitude and in phase. Nevertheless, the signal measured on the scalp and inside the brain at nearby locations showed a 10-fold difference in amplitude due to electrical insulation from the head. To further quantify the relationship between the scalp and intracerebral recordings, we used an approach correlating time-varying signals at the stimulation frequency across scalp and intracerebral channels. This analysis revealed a focused and right-lateralized correspondence between the scalp and intracerebral recordings that were specific to the face stimulation is more broadly distributed in various control situations. These results demonstrate the interest of a frequency tagging approach in characterizing the electrical propagation from brain sources to scalp EEG sensors and in identifying the cortical sources of brain functions from these recordings.

The developmental course of neural tuning to visual letter strings is unclear. Here we tested 39 children longitudinally, at the beginning of grade 1 (6.45 ± 0.33 years old) and 1 year after, with fast periodic visual stimulation in electroencephalography to assess the evolution of selective neural responses to letter strings and their relationship with emerging reading abilities. At both grades, frequency‐tagged letter strings were discriminated from pseudofont strings (i.e. letter‐selectivity) over the left occipito‐temporal cortex, with effects observed at the individual level in 62% of children. However, visual words were not discriminated from pseudowords (lexical access) at either grade. Following 1 year of schooling, letter‐selective responses showed a specific increase in amplitude, a more complex pattern of harmonics, and were located more anteriorly over the left occipito‐temporal cortex. Remarkably, at both grades, neural responses were highly significant at the individual level and correlated with individual reading scores. The amplitude increase in letter‐selective responses between grades was not found for discrimination responses of familiar keyboard symbols from pseudosymbols, and was not related to a general increase in visual stimulation responses. These findings demonstrate a rapid onset of left hemispheric letter selectivity, with 1 year of reading instruction resulting in increased emerging reading abilities and a clear quantitative and qualitative evolution within left hemispheric neural circuits for reading., A group of 39 young children were tested with FPVS‐EEG to understand changes in the left hemisphere when learning to read. After only 1 year of schooling, a quantitative and qualitative evolution in the selective neural responses to letters is found, independently of a general increase of visual stimulation responses.

The sudden inability to recognize individual faces following brain damage was first reported in a scientific journal 150 years ago and termed 'prosopagnosia' 70 years ago. While the term originally identified a face-selective neurological condition, it is now obscured by a sequence of imprecisions. First, prosopagnosia is routinely used to define symptoms of individual face recognition (IFR) difficulties in the context of visual object agnosia or other neurological conditions, or even in the normal population. Second, this over-expansive definition has lent support to a long-standing within-category recognition account of prosopagnosia, that is, that the impairment of IFR reflects a general impairment in recognizing within-category objects. However, stringent experimental studies of classical cases of prosopagnosia following brain damage show that their core impairment is not in recognizing physically similar exemplars within non-face object categories. Instead, the impairment presents specifically for recognizing exemplars of the category of faces. Moreover, compared to typical observers, the impairment appears even more severe for recognizing individual faces against physically dissimilar than similar distractors. Here, I argue that we need to limit accordingly our definition of prosopagnosia to a clinical (i.e., neurological) condition in which there is no basic-level object recognition impairment. Other criteria for prosopagnosia are proposed, with the hope that this conservative definition enables the study of human IFR processes in isolation, and supports progress in understanding the nature of these processes.

The neural basis of face categorization has been widely investigated with functional magnetic resonance imaging (fMRI), identifying a set of face-selective local regions in the ventral occipitotemporal cortex (VOTC). However, indirect recording of neural activity with fMRI is associated with large fluctuations of signal across regions, often underestimating face-selective responses in the anterior VOTC. While direct recording of neural activity with subdural grids of electrodes (electrocorticography, ECoG) or depth electrodes (stereotactic electroencephalography, SEEG) offers a unique opportunity to fill this gap in knowledge, these studies rather reveal widely distributed face-selective responses. Moreover, intracranial recordings are complicated by interindividual variability in neuroanatomy, ambiguity in definition, and quantification of responses of interest, as well as limited access to sulci with ECoG. Here, we propose to combine SEEG in large samples of individuals with fast periodic visual stimulation to objectively define, quantify, and characterize face categorization across the whole VOTC. This approach reconciles the wide distribution of neural face categorization responses with their (right) hemispheric and regional specialization, and reveals several face-selective regions in anterior VOTC sulci. We outline the challenges of this research program to understand the neural basis of face categorization and high-level visual recognition in general.

Electrical brain stimulation can provide important information about the functional organization of the human visual cortex. Here, we report the visual phenomena evoked by a large number (562) of intracerebral electrical stimulations performed at low-intensity with depth electrodes implanted in the occipito-parieto-temporal cortex of 22 epileptic patients. Focal electrical stimulation evoked primarily visual hallucinations with various complexities: simple (spot or blob), intermediary (geometric forms), or complex meaningful shapes (faces); visual illusions and impairments of visual recognition were more rarely observed. With the exception of the most posterior cortical sites, the probability of evoking a visual phenomenon was significantly higher in the right than the left hemisphere. Intermediary and complex hallucinations, illusions, and visual recognition impairments were almost exclusively evoked by stimulation in the right hemisphere. The probability of evoking a visual phenomenon decreased substantially from the occipital pole to the most anterior sites of the temporal lobe, and this decrease was more pronounced in the left hemisphere. The greater sensitivity of the right occipito-parieto-temporal regions to intracerebral electrical stimulation to evoke visual phenomena supports a predominant role of right hemispheric visual areas from perception to recognition of visual forms, regardless of visuospatial and attentional factors.

Previous studies have shown that acquired prosopagnosia is characterized by impairment at holistic/configural processing. However, this view is essentially supported by studies performed with patients whose face recognition difficulties are part of a more general visual (integrative) agnosia. Here, we tested the patient PS, a case of acquired prosopagnosia whose face-specific recognition difficulties have been related to the inability to process individual faces holistically (absence of inversion, composite, and whole-part effects with faces). Here, we show that in contrast to this impairment, the patient presents with an entirely normal response profile in a Navon hierarchical letter task: she was as fast as normal controls, faster to identify global than local letters, and her sensitivity to global interference during identification of local letters was at least as large as normal observers. These observations indicate that holistic processing as measured with global/local interference in the Navon paradigm is functionally distinct from the ability to perceive an individual face holistically.

Neuroimaging studies of humans have provided inconsistent evidence with respect to the response properties of the fusiform face area (FFA). It has been claimed that neural populations within this region are sensitive to subtle differences between individual faces only when they are perceived as distinct identities [P. Rotshtein et al. (2005)Nature Neuroscience, 8, 107-113]. However, sensitivity to subtle changes of identity was found in previous studies using unfamiliar faces, for which categorical perception is less pronounced. Using functional magnetic resonance adaptation and morph continua of personally familiar faces, we investigated sensitivity to subtle changes between faces that were located either on the same or opposite sides of a categorical perceptual boundary. We found no evidence for categorical perception within the FFA, which exhibited reliable sensitivity to subtle changes of face identity whether these were perceived as distinct identities, or not. On the contrary, both the posterior superior temporal sulcus and prefrontal cortex exhibited categorical perception, as subtle changes between faces perceived as different identities yielded larger release from adaptation than those perceived as the same identity. These observations suggest that, whereas the FFA discriminates subtle physical changes of personally familiar faces, other regions encode faces in a categorical fashion.

It is well known that adults' face recognition is characterized by an 'other-race effect' (ORE; see Meissner & Brigham, 2001), but few studies have investigated this ORE during the development of the face processing system. Here we examined the role of experience with other-race faces during childhood by testing a group of 6- to 14-year-old Asian children adopted between 2 and 26 months in Caucasian families living in Western Europe, as well as a group of age-matched Caucasian children. The latter group showed a strong ORE in favour of own-race faces that was stable from 6 to 14 years of age. The adopted participants did not show a significant reversal of the ORE, unlike a recently reported study (Sangrigoli et al., 2005), but rather comparable results with Asian and Caucasian faces. Their pattern of performance was neither influenced by their age of adoption, nor by the amount of experience they accumulated during childhood with other-race faces. These results indicate that the balance of performance with Asian and Caucasian faces can be modulated, but not completely reversed, in children whose exposure to own- and other-race faces changes drastically during the period of maturation of the face recognition system, depending on the length of exposure to the new face race. Overall, experience appears to be crucial during childhood to shape the face recognition system towards the most predominant morphologies of faces present in the environment.

Recent studies have shown that same-race (SR) faces are processed more holistically than other-race (OR) faces, a difference that may underlie the greater difficulty at recognizing OR than SR faces (the "other-race effect"). This article provides original evidence suggesting that the holistic processing of faces may be sensitive to the observers' racial categorization of the face. In Experiment 1, Caucasian participants performed a face-composite task with Caucasian faces, Asian faces, and racially ambiguous morphed face stimuli. Identical morphed face stimuli were processed more holistically when categorized as SR than as OR faces. Experiment 2 further suggests that this finding was not underlain by strategic or training effects. Overall, these results support the view that one's categorization of a face as belonging to the same or another race plays a critical role in the holistic processing of this face.

Behavioral studies have shown that two different morphed faces belonging to the same identity are harder to discriminate than two faces stemming from two different identities. The temporal course of this categorical perception effect has been explored through event-related potentials. Three kinds of pairs were presented in a matching task: (1) two different morphed faces representing the same identity (within), (2) two other faces representing two different identities (between), and (3) two identical morphed faces (same). Following the second face onset in the pair, the amplitude of the right occipitotemporal negativity (N170) was reduced for within and same pairs as compared with between pairs, suggesting an identity priming effect. We also observed a modulation of the P3b wave, as the amplitude of the responses for within pairs was higher than for between and same pairs, suggesting a higher complexity of the task for within pairs. These results indicate that categorical perception of human faces has a perceptual origin in the right occipitotemporal hemisphere.