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Face-selective regions in the human ventral occipito-temporal cortex (VOTC) have been defined for decades mainly with functional magnetic resonance imaging. This face-selective VOTC network is traditionally divided in a posterior 'core' system thought to subtend face perception, and regions of the anterior temporal lobe as a semantic memory component of an extended general system. In between these two putative systems lies the anterior fusiform gyrus and surrounding sulci, affected by magnetic susceptibility artifacts. Here we suggest that this methodological gap overlaps with and contributes to a conceptual gap between (visual) perception and semantic memory for faces. Filling this gap with intracerebral recordings and direct electrical stimulation reveals robust face-selectivity in the anterior fusiform gyrus and a crucial role of this region, especially in the right hemisphere, in identity recognition for both familiar and unfamiliar faces. Based on these observations, we propose an integrated theoretical framework for human face (identity) recognition according to which face-selective regions in the anterior fusiform gyrus join the dots between posterior and anterior cortical face memories., Competing Interests: Declaration of Competing Interest The authors have no conflict of interest to declare., (Copyright © 2024 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Understanding how the human brain recognizes faces is a primary scientific goal in cognitive neuroscience. Given the limitations of the monkey model of human face recognition, a key approach in this endeavor is the recording of electrophysiological activity with electrodes implanted inside the brain of human epileptic patients. However, this approach faces a number of challenges that must be overcome for meaningful scientific knowledge to emerge. Here we synthesize a 10 year research program combining the recording of intracerebral activity (StereoElectroEncephaloGraphy, SEEG) in the ventral occipito-temporal cortex (VOTC) of large samples of participants and fast periodic visual stimulation (FPVS), to objectively define, quantify, and characterize the neural basis of human face recognition. These large-scale studies reconcile the wide distribution of neural face recognition activity with its (right) hemispheric and regional specialization and extend face-selectivity to anterior regions of the VOTC, including the ventral anterior temporal lobe (VATL) typically affected by magnetic susceptibility artifacts in functional magnetic resonance imaging (fMRI). Clear spatial dissociations in category-selectivity between faces and other meaningful stimuli such as landmarks (houses, medial VOTC regions) or written words (left lateralized VOTC) are found, confirming and extending neuroimaging observations while supporting the validity of the clinical population tested to inform about normal brain function. The recognition of face identity - arguably the ultimate form of recognition for the human brain - beyond mere differences in physical features is essentially supported by selective populations of neurons in the right inferior occipital gyrus and the lateral portion of the middle and anterior fusiform gyrus. In addition, low-frequency and high-frequency broadband iEEG signals of face recognition appear to be largely concordant in the human association cortex. We conclude by outlining the challenges of this research program to understand the neural basis of human face recognition in the next 10 years.

Decoding emotions on others' faces is one of the most important functions of the human brain, which has been widely studied in cognitive neuroscience. However, the precise time course of facial expression categorization in the human brain is still a matter of debate. Here we used an original paradigm to measure categorical perception of facial expression changes during event-related potentials (ERPs) recording, in which a face stimulus dynamically switched either to a different expression (between-category condition) or to the same expression (within-category condition), the physical distance between the two successive faces being equal across conditions. The switch between faces generated a negative differential potential peaking at around 160 ms over occipito-temporal regions, similar in term of latency and topography to the well-known face-selective N170 component. This response was larger in the condition where the switch occurred between faces that were perceived as having different facial expressions compared to the same expression. In addition, happy expressions were categorized around 20 ms faster than fearful expressions (respectively, 135 and 156 ms). These findings provide evidence that changes of facial expressions are categorically perceived as early as 160 ms following stimulus onset over the occipito-temporal cortex., Competing Interests: Declarations of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

The extent to which faces and written words share neural circuitry in the human brain is actively debated. Here, we compare face-selective and word-selective responses in a large group of patients (N = 37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. non-face visual objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated with frequency-tagging. Critically, this sensitive approach allows to objectively quantify category-selective neural responses and disentangle them from general visual responses. About 70% of significant electrode contacts show either face-selectivity or word-selectivity only, with the expected right and left hemispheric dominance, respectively. Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci, respectively. In the 30% of overlapping face- and word-selective contacts across the VOTC or in the FG and surrounding sulci, between-category-selective amplitudes (faces vs. words) show no-to-weak correlations, despite strong correlations in both the within-category-selective amplitudes (face-face, word-word) and the general visual responses to words and faces. Overall, these observations support the view that category-selective circuitry for faces and written words is largely dissociated in the human adult VOTC., (© 2021. The Author(s).)

Rapid individuation of conspecifics' faces is ecologically important in the human species, whether the face belongs to a familiar or unfamiliar individual. Here we tested a large group (N = 69) of epileptic patients implanted with intracerebral electrodes throughout the ventral occipito-temporal cortex (VOTC). We used a frequency-tagging visual stimulation paradigm optimized to objectively measure face individuation with direct neural recordings. This enabled providing an extensive map of the significantly larger neural responses to upright than to inverted unfamiliar faces, i.e. reflecting visual face individuation processes that go beyond physical image differences. These high-level face individuation responses are both distributed and anatomically confined to a strip of cortex running from the inferior occipital gyrus all along the lateral fusiform gyrus, with a large right hemispheric dominance. Importantly, face individuation responses are limited anteriorly to the bilateral anterior fusiform gyrus and surrounding sulci, with a near absence of significant responses in the extensively sampled temporal pole. This large-scale mapping provides original evidence that face individuation is supported by a distributed yet anatomically constrained population of neurons in the human VOTC, and highlights the importance of probing this function with face stimuli devoid of associated semantic, verbal and affective information., (Copyright © 2020. Published by Elsevier Inc.)

Developmental accounts of autism spectrum disorder (ASD) state that infants and children with ASD are spontaneously less attracted by and less proficient in processing social stimuli such as faces. This is hypothesized to partly underlie social communication difficulties in ASD. While in some studies a reduced preference for social stimuli has been shown in individuals with ASD, effect sizes are moderate and vary across studies, stimuli, and designs. Eye tracking, often the methodology of choice to study social preference, conveys information about overt orienting processes but conceals covert attention, possibly resulting in an underestimation of the effects. In this study, we recorded eye tracking and electroencephalography (EEG) during fast periodic visual stimulation to address this issue. We tested 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ. Streams of variable images of faces were presented at 6 Hz alongside images of houses presented at 7.5 Hz or vice versa, while children were engaged in an orthogonal task. While frequency-tagged neural responses were larger in response to faces than simultaneously presented houses in both groups, this effect was much larger in TD boys than in boys with ASD. This group difference in saliency of social versus non-social processing is significant after 5 sec of stimulus presentation and holds throughout the entire trial. Although there was no interaction between group and stimulus category for simultaneously recorded eye-tracking data, eye tracking and EEG measures were strongly correlated. We conclude that frequency-tagging EEG, allowing monitoring of both overt and covert processes, provides a fast, objective and reliable measure of decreased preference for social information in ASD., (Copyright © 2019. Published by Elsevier Ltd.)

Background: Individuals with autism spectrum disorder (ASD) are characterized by impairments in social communication and interaction. Although difficulties at processing social signals from the face in ASD have been observed and emphasized for many years, there is a lot of inconsistency across both behavioral and neural studies., Methods: We recorded scalp electroencephalography (EEG) in 23 8-to-12 year old boys with ASD and 23 matched typically developing boys using a fast periodic visual stimulation (FPVS) paradigm, providing objective (i.e., frequency-tagged), fast (i.e., few minutes) and highly sensitive measures of rapid face categorization, without requiring any explicit face processing task. We tested both the sensitivity to rapidly (i.e., at a glance) categorize faces among other objects and to individuate unfamiliar faces., Outcomes: While general neural synchronization to the visual stimulation and neural responses indexing generic face categorization were undistinguishable between children with ASD and typically developing controls, neural responses indexing individual face discrimination over the occipito-temporal cortex were substantially reduced in the individuals with ASD. This difference vanished when faces were presented upside-down, due to the lack of significant face inversion effect in ASD., Interpretation: These data provide original evidence for a selective high-level impairment in individual face discrimination in ASD in an implicit task. The objective and rapid assessment of this function opens new perspectives for ASD diagnosis in clinical settings., (Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.)

We report a comprehensive cartography of selective responses to visual letters and words in the human ventral occipito-temporal cortex (VOTC) with direct neural recordings, clarifying key aspects of the neural basis of reading. Intracerebral recordings were performed in a large group of patients ( n = 37) presented with visual words inserted periodically in rapid sequences of pseudofonts, nonwords, or pseudowords, enabling classification of responses at three levels of word processing: letter, prelexical, and lexical. While letter-selective responses are found in much of the VOTC, with a higher proportion in left posterior regions, prelexical/lexical responses are confined to the middle and anterior sections of the left fusiform gyrus. This region overlaps with and extends more anteriorly than the visual word form area typically identified with functional magnetic resonance imaging. In this region, prelexical responses provide evidence for populations of neurons sensitive to the statistical regularity of letter combinations independently of lexical responses to familiar words. Despite extensive sampling in anterior ventral temporal regions, there is no hierarchical organization between prelexical and lexical responses in the left fusiform gyrus. Overall, distinct word processing levels depend on neural populations that are spatially intermingled rather than organized according to a strict postero-anterior hierarchy in the left VOTC., Competing Interests: The authors declare no conflict of interest.

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., (© 2018 New York Academy of Sciences.)

Although humans discriminate natural images of faces from other categories at a single glance, clarifying the neural specificity and spatio-temporal dynamics of this process without low-level visual confounds remains a challenge. We recorded high-density scalp electroencephalogram while presenting natural images of various objects at a fast periodic rate (5.88images/s). In different stimulation sequences, numerous variable exemplars of three categories associated with cortical specialization in neuroimaging - faces, body parts, or houses - appeared every five images (5.88Hz/5=1.18Hz). In these fast periodic visual stimulation (FPVS) sequences, common low- and high-level visual processes between these categories and other objects are captured at the 5.88Hz frequency, while high-level category-selective responses are objectively quantified at the 1.18Hz frequency and harmonics. Category-selective responses differed quantitatively and qualitatively between faces, body parts and houses. First, they were much larger (2-4 times) for faces over the whole scalp. Second, specific and reliable scalp topographical maps of category-selective responses pointed to distinct principle neural sources for faces (ventral occipito-temporal), body parts (lateral occipito-temporal) and houses (dorso-medial occipital). Category-selective EEG responses were found at multiple time-windows from 110 to 600ms post-stimulus onset. Faces elicited the most complex spatio-temporal profile with up to four selective responses, although body parts and houses also elicited selective responses more complex than previously described. These observations indicate that a single glance at natural face images inserted in a rapid stream of natural objects generates a quantitatively and qualitatively unique category-selective spatio-temporal signature in occipito-temporal cortical areas of the human brain., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Human neuroimaging studies have identified a network of distinct face-selective regions in the ventral occipito-temporal cortex (VOTC), with a right hemispheric dominance. To date, there is no evidence for this hemispheric and regional specialization with direct measures of brain activity. To address this gap in knowledge, we recorded local neurophysiological activity from 1,678 contact electrodes implanted in the VOTC of a large group of epileptic patients (n = 28). They were presented with natural images of objects at a rapid fixed rate (six images per second: 6 Hz), with faces interleaved as every fifth stimulus (i.e., 1.2 Hz). High signal-to-noise ratio face-selective responses were objectively (i.e., exactly at the face stimulation frequency) identified and quantified throughout the whole VOTC. Face-selective responses were widely distributed across the whole VOTC, but also spatially clustered in specific regions. Among these regions, the lateral section of the right middle fusiform gyrus showed the largest face-selective response by far, offering, to our knowledge, the first supporting evidence of two decades of neuroimaging observations with direct neural measures. In addition, three distinct regions with a high proportion of face-selective responses were disclosed in the right ventral anterior temporal lobe, a region that is undersampled in neuroimaging because of magnetic susceptibility artifacts. A high proportion of contacts responding only to faces (i.e., "face-exclusive" responses) were found in these regions, suggesting that they contain populations of neurons involved in dedicated face-processing functions. Overall, these observations provide a comprehensive mapping of visual category selectivity in the whole human VOTC with direct neural measures.

Functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG) research have been influential in revealing the functional characteristics of category-selective responses in human ventral temporal cortex (VTC). One important, but unanswered, question is how these two types of measurements might be related with respect to the VTC. Here we examined which components of the ECoG signal correspond to the fMRI response by using a rare opportunity to measure both fMRI and ECoG responses from the same individuals to images of exemplars of various categories including faces, limbs, cars and houses. Our data reveal three key findings. First, we discovered that the coupling between fMRI and ECoG responses is frequency and time dependent. The strongest and most sustained correlation is observed between fMRI and high frequency broadband (HFB) ECoG responses (30-160 hz). In contrast, the correlation between fMRI and ECoG signals in lower frequency bands is temporally transient, where the correlation is initially positive, but then tapers off or becomes negative. Second, we find that the strong and positive correlation between fMRI and ECoG signals in all frequency bands emerges rapidly around 100 ms after stimulus onset, together with the onset of the first stimulus-driven neural signals in VTC. Third, we find that the spatial topology and representational structure of category-selectivity in VTC reflected in ECoG HFB responses mirrors the topology and structure observed with fMRI. These findings of a strong and rapid coupling between fMRI and HFB responses validate fMRI measurements of functional selectivity with recordings of direct neural activity and suggest that fMRI category-selective signals in VTC are associated with feed-forward neural processing., (Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.)

According to neuropsychological evidence, a distributed network of regions of the ventral visual pathway - from the lateral occipital cortex to the temporal pole - supports face recognition. However, functional magnetic resonance imaging (fMRI) studies have generally confined ventral face-selective areas to the posterior section of the occipito-temporal cortex, i.e., the inferior occipital gyrus occipital face area (OFA) and the posterior and middle fusiform gyrus fusiform face area (FFA). There is recent evidence that intracranial electrical stimulation of these areas in the right hemisphere elicits face matching and recognition impairments (i.e., prosopagnosia) as well as perceptual face distortions. Here we report a case of transient inability to recognize faces following electrical stimulation of the right anterior fusiform gyrus, in a region located anteriorly to the FFA. There was no perceptual face distortion reported during stimulation. Although no fMRI face-selective responses were found in this region due to a severe signal drop-out as in previous studies, intracerebral face-selective event-related potentials and gamma range electrophysiological responses were found at the critical site of stimulation. These results point to a causal role in face recognition of the right anterior fusiform gyrus and more generally of face-selective areas located beyond the "core" face-processing network in the right ventral temporal cortex. It also illustrates the diagnostic value of intracerebral electrophysiological recordings and stimulation in understanding the neural basis of face recognition and visual recognition in general., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Periodic presentation of visual stimuli leads to a robust electrophysiological response on the human scalp exactly at the periodic stimulation frequency, a response defined as a "steady-state visual evoked potential" (SSVEP, Regan, 1966). However, recent studies have shown that SSVEPs over the (right) occipito-temporal cortex are reduced when the same individual face is repeated at periodic rates of 3 to 9 Hz compared to when different faces are presented (Rossion, 2014). Here, we characterized the temporal dynamics of this repetition suppression effect. We presented different face identities at a rate of 5.88 Hz (stimulus onset asynchrony of 170 ms) for 15 s, followed by the repetition of the exact same face at this rate for 35 s. Compared to a stimulation sequence with different faces only, there was a large and specific decrease of the 5.88 Hz response when the same face was repeated at that rate. This effect was observed over the left and right occipito-temporal cortex, but not over medial occipital electrode sites where SSVEPs are typically measured. In the right hemisphere, this decrease occurred abruptly, i.e., within half a second following the introduction of the same-identity stimulation, with no further decrease until the end of the stimulation. These observations indicate that the SSVEP recorded over high-level visual areas to periodic stimulation is not steady but rather adapts immediately and fully following the repetition of the same individual face, supporting a bottom-up, stimulus-driven account of repetition suppression effects., (Copyright © 2015 Elsevier B.V. All rights reserved.)

We designed a fast periodic visual stimulation approach to identify an objective signature of face categorization incorporating both visual discrimination (from nonface objects) and generalization (across widely variable face exemplars). Scalp electroencephalographic (EEG) data were recorded in 12 human observers viewing natural images of objects at a rapid frequency of 5.88 images/s for 60 s. Natural images of faces were interleaved every five stimuli, i.e., at 1.18 Hz (5.88/5). Face categorization was indexed by a high signal-to-noise ratio response, specifically at an oddball face stimulation frequency of 1.18 Hz and its harmonics. This face-selective periodic EEG response was highly significant for every participant, even for a single 60-s sequence, and was generally localized over the right occipitotemporal cortex. The periodicity constraint and the large selection of stimuli ensured that this selective response to natural face images was free of low-level visual confounds, as confirmed by the absence of any oddball response for phase-scrambled stimuli. Without any subtraction procedure, time-domain analysis revealed a sequence of differential face-selective EEG components between 120 and 400 ms after oddball face image onset, progressing from medial occipital (P1-faces) to occipitotemporal (N1-faces) and anterior temporal (P2-faces) regions. Overall, this fast periodic visual stimulation approach provides a direct signature of natural face categorization and opens an avenue for efficiently measuring categorization responses of complex visual stimuli in the human brain., (© 2015 ARVO.)

During intracerebral stimulation of the right inferior occipital cortex, a patient with refractory epilepsy was transiently 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 original 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 functional 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., (Copyright © 2014 Elsevier Inc. All rights reserved.)

The specificity of face perception is thought to reside both in its dramatic vulnerability to picture-plane inversion and its strong reliance on horizontally oriented image content. Here we asked when in the visual processing stream face-specific perception is tuned to horizontal information. We measured the behavioral performance and scalp event-related potentials (ERP) when participants viewed upright and inverted images of faces and cars (and natural scenes) that were phase-randomized in a narrow orientation band centered either on vertical or horizontal orientation. For faces, the magnitude of the inversion effect (IE) on behavioral discrimination performance was significantly reduced for horizontally randomized compared to vertically or nonrandomized images, confirming the importance of horizontal information for the recruitment of face-specific processing. Inversion affected the processing of nonrandomized and vertically randomized faces early, in the N170 time window. In contrast, the magnitude of the N170 IE was much smaller for horizontally randomized faces. The present research indicates that the early face-specific neural representations are preferentially tuned to horizontal information and offers new perspectives for a description of the visual information feeding face-specific perception.

Whether the development of face recognition abilities truly reflects changes in how faces, specifically, are perceived, or rather can be attributed to more general perceptual or cognitive development, is debated. Event-related potential (ERP) recordings on the scalp offer promise for this issue because they allow brain responses to complex visual stimuli to be relatively well isolated from other sensory, cognitive and motor processes. ERP studies in 5- to 16-year-old children report large age-related changes in amplitude, latency (decreases) and topographical distribution of the early visual components, the P1 and the occipito-temporal N170. To test the face specificity of these effects, we recorded high-density ERPs to pictures of faces, cars, and their phase-scrambled versions from 72 children between the ages of 4 and 17, and a group of adults. We found that none of the previously reported age-dependent changes in amplitude, latency or topography of the P1 or N170 were specific to faces. Most importantly, when we controlled for age-related variations of the P1, the N170 appeared remarkably similar in amplitude and topography across development, with much smaller age-related decreases in latencies than previously reported. At all ages the N170 showed equivalent face-sensitivity: it had the same topography and right hemisphere dominance, it was absent for meaningless (scrambled) stimuli, and larger and earlier for faces than cars. The data also illustrate the large amount of inter-individual and inter-trial variance in young children's data, which causes the N170 to merge with a later component, the N250, in grand-averaged data. Based on our observations, we suggest that the previously reported "bi-fid" N170 of young children is in fact the N250. Overall, our data indicate that the electrophysiological markers of face-sensitive perceptual processes are present from 4 years of age and do not appear to change throughout development.

Identifying a facial feature (e.g. the eyes) is influenced by the position and identity of other features (e.g. the mouth) of the face, supporting the view that an individual face is represented as a whole in the human brain. To clarify how early in the time-course of face processing this holistic individual representation is accessed we recorded event-related potentials during an adaptation paradigm of the composite face illusion (CFI). Observers performed a matching task on top halves of two faces presented sequentially. For each face pair, top and bottom face halves could be both identical, both different, or only the bottom half differed. The signal was larger over the right occipito-temporal cortex at about 160 ms (N170) when the attended top half differed between the two faces than when identical top halves were repeated. Crucially, a larger N170 was also found when the top halves of the two faces were the same, yet the observers had the illusion that they differed (CFI). This effect was not found when the two face halves were spatially misaligned. These observations indicate that the earliest perceptual representation of an individual face in the human brain is holistic rather than based on independent face parts.

A recent event-related potential (ERP) study showed that the occipitotemporal component N170 recorded to a face stimulus appearing in the peripheral visual field is strongly reduced when subjects are concurrently fixating another face stimulus. This suggests that concurrently presented face stimuli compete for neural representation in the occipitotemporal cortex between 100 and 200 ms following stimulus onset. We tested whether this competition can be observed for a foveally presented face stimulus appearing next to either two peripheral face pictures or two peripheral control stimuli. The N170 in response to the fixated central face stimulus was substantially reduced (approximately 20% of signal) when it was presented next to peripheral face stimuli. The response suppression was smaller in magnitude than in a previous study where the competing stimulus was fixated and the target stimulus appeared in the periphery. Besides providing a better control for attentional and eye movement confounds, the concurrent stimulation paradigm for fixated face stimuli in ERPs offers a powerful tool to investigate the time course and the nature of the interactions between face and nonface object representations.