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A major scientific objective of cognitive neuroscience is to define cortico-cortical functional connections supporting cognitive functions. Here, we use an original approach combining frequency-tagging and direct electrical stimulation (DES) to test for bidirectional and cross-hemispheric category-specific modulations within the human cortical face network. A unique patient bilaterally implanted with depth electrodes in multiple face-selective cortical regions of the ventral occipito-temporal cortex (VOTC) was shown 70 s sequences of variable natural object images at a 6 Hz rate, objectively identifying deviant face-selective neural activity at 1.2 Hz (i.e., every five images). Concurrent electrical stimulation was separately applied for 10 seconds on four independently defined face-selective sites in the right and left VOTC. Upon stimulation, we observed reduced or even abolished face-selective neural activity locally and, most interestingly, at distant VOTC recording sites. Remote DES effects were found up to the anterior temporal lobe (ATL) in both forward and backward directions along the VOTC, as well as across the two hemispheres. This reduction was specific to face-selective neural activity, with the general 6 Hz visual response being mostly unaffected. Overall, these results shed light on the functional connectivity of the cortical face-selective network, supporting its non-hierarchical organization as well as bidirectional effective category-selective connections between posterior ‘core’ regions and the ATL. They also pave the way for widespread and systematic development of this approach to better understand the functional and effective connectivity of human brain networks.

Abstract Human adults associate different views of an identity much better for familiar than for unfamiliar faces. However, a robust and consistent neural index of this behavioral face identity familiarity effect (FIFE)—not found in non-human primate species—is lacking. Here we provide such a neural FIFE index, measured implicitly and with one fixation per face. Fourteen participants viewed 70 s stimulation sequences of a large set (n = 40) of widely variable natural images of a face identity at a rate of 6 images/second (6 Hz). Different face identities appeared every 5th image (1.2 Hz). In a sequence, face images were either familiar (i.e., famous) or unfamiliar, participants performing a non-periodic task unrelated to face recognition. The face identity recognition response identified at 1.2 Hz over occipital-temporal regions in the frequency-domain electroencephalogram was 3.4 times larger for familiar than unfamiliar faces. The neural response to familiar faces—which emerged at about 180 ms following face onset—was significant in each individual but a case of prosopdysgnosia. Besides potential clinical and forensic applications to implicitly measure one’s knowledge of a face identity, these findings open new perspectives to clarify the neurofunctional source of the FIFE and understand the nature of human face identity recognition.

Abstract Faces are critical for social interactions and their recognition constitutes one of the most important and challenging functions of the human brain. While neurons responding selectively to faces have been recorded for decades in the monkey brain, face-selective neural activations have been reported with neuroimaging primarily in the human midfusiform gyrus. Yet, the cellular mechanisms producing selective responses to faces in this hominoid neuroanatomical structure remain unknown. Here we report single neuron recordings performed in 5 human subjects (1 male, 4 females) implanted with intracerebral microelectrodes in the face-selective midfusiform gyrus, while they viewed pictures of familiar and unknown faces and places. We observed similar responses to faces and places at the single cell level, but a significantly higher number of neurons responding to faces, thus offering a mechanistic account for the face-selective activations observed in this region. Although individual neurons did not respond preferentially to familiar faces, a population level analysis could consistently determine whether or not the faces (but not the places) were familiar, only about 50 ms after the initial recognition of the stimuli as faces. These results provide insights into the neural mechanisms of face processing in the human brain.

Face identity recognition (FIR) in humans is supported by specialized neural processes whose function is spectacularly impaired when simply turning a face upside-down: the face inversion effect (FIE). While the FIE appears to have a slow developmental course, little is known about the plasticity of the neural processes involved in this effect—and in FIR in general—at adulthood. Here, we investigate whether extensive training (2 weeks, ~16 h) in young human adults discriminating a large set of unfamiliar inverted faces can reduce an implicit neural marker of the FIE for a set of entirely novel faces. In all, 28 adult observers were trained to individuate 30 inverted face identities presented under different depth-rotated views. Following training, we replicate previous behavioral reports of a significant reduction (56% relative accuracy rate) in the behavioral FIE as measured with a challenging four-alternative delayed-match-to-sample task for individual faces across depth-rotated views. Most importantly, using EEG together with a validated frequency tagging approach to isolate a neural index of FIR, we observe the same substantial (56%) reduction in the neural FIE at the expected occipito-temporal channels. The reduction in the neural FIE correlates with the reduction in the behavioral FIE at the individual participant level. Overall, we provide novel evidence suggesting a substantial degree of plasticity in processes that are key for face identity recognition in the adult human brain.

Non-human primate (NHP) neuroimaging can provide essential insights into the neural basis of human cognitive functions. While functional magnetic resonance imaging (fMRI) localizers can play an essential role in reaching this objective (Russ et al., 2021), they often differ substantially across species in terms of paradigms, measured signals, and data analysis, biasing the comparisons. Here we introduce a functional frequency-tagging face localizer for NHP imaging, successfully developed in humans and outperforming standard face localizers (Gao et al., 2018). FMRI recordings were performed in two awake macaques. Within a rapid 6 Hz stream of natural non-face objects images, human or monkey face stimuli were presented in bursts every 9 s. We also included control conditions with phase-scrambled versions of all images. As in humans, face-selective activity was objectively identified and quantified at the peak of the face-stimulation frequency (0.111 Hz) and its second harmonic (0.222 Hz) in the Fourier domain. Focal activations with a high signal-to-noise ratio were observed in regions previously described as face-selective, mainly in the STS (clusters PL, ML, MF; also, AL, AF), both for human and monkey faces. Robust face-selective activations were also found in the prefrontal cortex of one monkey (PVL and PO clusters). Face-selective neural activity was highly reliable and excluded all contributions from low-level visual cues contained in the amplitude spectrum of the stimuli. These observations indicate that fMRI frequency-tagging provides a highly valuable approach to objectively compare human and monkey visual recognition systems within the same framework.

In vivo intracranial recordings of neural activity offer a unique opportunity to understand human brain function. Intracranial electrophysiological (iEEG) activity related to sensory, cognitive or motor events manifests mostly in two types of signals: event-related local field potentials in lower frequency bands (30 Hz, High frequency, HF). While most current studies rely exclusively on HF, thought to be more focal and closely related to spiking activity, the relationship between HF and LF signals is unclear, especially in human associative cortex. Here, we provide a large-scale in-depth investigation of the spatial and functional relationship between these 2 signals based on intracranial recordings from 121 individual brains (8000 recording sites). We measure category-selective responses to complex ecologically salient visual stimuli – human faces – across a wide cortical territory in the ventral occipito-temporal cortex (VOTC), with a frequency-tagging method providing high signal-to-noise ratio (SNR) and the same objective quantification of signal and noise for the two frequency ranges. While LF face-selective activity has higher SNR across the VOTC, leading to a larger number of significant electrode contacts especially in the anterior temporal lobe, LF and HF display highly similar spatial, functional, and timing properties. Specifically, and contrary to a widespread assumption, our results point to nearly identical spatial distribution and local spatial extent of LF and HF activity at equal SNR. These observations go a long way towards clarifying the relationship between the two main iEEG signals and reestablish the informative value of LF iEEG to understand human brain function.

Infants’ ability to discriminate facial expressions has been widely explored, but little is known about the rapid and automatic ability to discriminate a given expression against many others in a single experiment. Here we investigated the development of facial expression discrimination in infancy with fast periodic visual stimulation coupled with scalp electroencephalography (EEG). EEG was recorded in eighteen 3.5- and eighteen 7-month-old infants presented with a female face expressing disgust, happiness, or a neutral emotion (in different stimulation sequences) at a base stimulation frequency of 6 Hz. Pictures of the same individual expressing other emotions (either anger, disgust, fear, happiness, sadness, or neutrality, randomly and excluding the expression presented at the base frequency) were introduced every six stimuli (at 1 Hz). Frequency-domain analysis revealed an objective (i.e., at the predefined 1-Hz frequency and harmonics) expression-change brain response in both 3.5- and 7-month-olds, indicating the visual discrimination of various expressions from disgust, happiness and neutrality from these early ages. At 3.5 months, the responses to the discrimination from disgust and happiness expressions were located mainly on medial occipital sites, whereas a more lateral topography was found for the response to the discrimination from neutrality, suggesting that expression discrimination from an emotionally neutral face relies on distinct visual cues than discrimination from a disgust or happy face. Finally, expression discrimination from happiness was associated with a reduced activity over posterior areas and an additional response over central frontal scalp regions at 7 months as compared to 3.5 months. This result suggests developmental changes in the processing of happiness expressions as compared to negative/neutral ones within this age range.

Brain regions located between the right fusiform face area (FFA) in the middle fusiform gyrus and the temporal pole may play a critical role in human face identity recognition but their investigation is limited by a large signal drop-out in functional magnetic resonance imaging (fMRI). Here we report an original case who is suddenly unable to recognize the identity of faces when electrically stimulated on a focal location inside this intermediate region of the right anterior fusiform gyrus. The reliable transient identity recognition deficit occurs without any change of percept, even during nonverbal face tasks (i.e., pointing out the famous face picture among three options; matching pictures of unfamiliar or familiar faces for their identities), and without difficulty at recognizing visual objects or famous written names. The effective contact is associated with the largest frequency-tagged electrophysiological signals of face-selectivity and of familiar and unfamiliar face identity recognition. This extensive multimodal investigation points to the right anterior fusiform gyrus as a critical hub of the human cortical face network, between posterior ventral occipito-temporal face-selective regions directly connected to low-level visual cortex, the medial temporal lobe involved in generic memory encoding, and ventral anterior temporal lobe regions holding semantic associations to people's identity.

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.

Seeing a face in the real world provokes a host of automatic categorisations related to sex, emotion, identity, and more. Such individual facets of human face recognition have been extensively examined using overt categorisation judgements, yet their relative informational dependencies during the same face encounter are comparatively unknown. Here we used EEG to assess how increasing access to sensory input governs two ecologically relevant brain functions elicited by seeing a face: Distinguishing faces and nonfaces, and recognising people we know. Observers viewed a large set of natural images that progressively increased in either image duration (experiment 1) or spatial frequency content (experiment 2). We show that in the absence of an explicit categorisation task, the human brain requires less sensory input to categorise a stimulus as a face than it does to recognise whether that face is familiar. Moreover, where sensory thresholds for distinguishing faces/nonfaces were remarkably consistent across observers, there was high inter-individual variability in the lower informational bound for familiar face recognition, underscoring the neurofunctional distinction between these categorisation functions. By i) indexing a form of face recognition that goes beyond simple low-level differences between categories, and ii) tapping multiple recognition functions elicited by the same face encounters, the information minima we report bear high relevance to real-world face encounters, where the same stimulus is categorised along multiple dimensions at once. Thus, our finding of lower informational requirements for generic vs. familiar face recognition constitutes some of the strongest evidence to date for the intuitive notion that sensory input demands should be lower for recognising face category than face identity.

Conceptual knowledge allows the categorisation of items according to their meaning beyond their physical similarities. This ability to respond to different stimuli (e.g., a leek, a cabbage, etc.) based on similar semantic representations (e.g., belonging to the vegetable category) is particularly important for language processing, because word meaning and the stimulus form are unrelated. The neural basis of this core human ability is debated and is complicated by the strong reliance of most neural measures on explicit tasks, involving many non-semantic processes. Here we establish an implicit method, i.e., fast periodic visual stimulation (FPVS) coupled with electroencephalography (EEG), to study neural conceptual categorisation processes with written word stimuli. Fourteen neurotypical participants were presented with different written words belonging to the same semantic category (e.g., different animals) alternating at 4 Hz rate. Words from a different semantic category (e.g., different cities) appeared every 4 stimuli (i.e., at 1 Hz). Following a few minutes of recording, objective electrophysiological responses at 1 Hz, highlighting the human brain's ability to implicitly categorize stimuli belonging to distinct conceptual categories, were found over the left occipito-temporal region. Topographic differences were observed depending on whether the periodic change involved living items, associated with relatively more ventro-temporal activity as compared to non-living items associated with relatively more dorsal posterior activity. Overall, this study demonstrates the validity and high sensitivity of an implicit frequency-tagged marker of word-based semantic memory abilities.

In humans, face-processing relies on a network of brain regions predominantly in the right occipito-temporal cortex. We tested congenitally deaf (CD) signers and matched hearing controls (HC) to investigate the experience dependence of the cortical organization of face processing. Specifically, we used EEG frequency-tagging to evaluate: (1) Face-Object Categorization, (2) Emotional Facial-Expression Discrimination and (3) Individual Face Discrimination. The EEG was recorded to visual stimuli presented at a rate of 6 Hz, with oddball stimuli at a rate of 1.2 Hz. In all three experiments and in both groups, significant face discriminative responses were found. Face-Object categorization was associated to a relative increased involvement of the left hemisphere in CD individuals compared to HC individuals. A similar trend was observed for Emotional Facial-Expression discrimination but not for Individual Face Discrimination. Source reconstruction suggested a greater activation of the auditory cortices in the CD group for Individual Face Discrimination. These findings suggest that the experience dependence of the relative contribution of the two hemispheres as well as crossmodal plasticity vary with different aspects of face processing.

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.

Visual categorization is integral for our interaction with the natural environment. In this process, similar selective responses are produced to a class of variable visual inputs. Whether categorization is supported by partial (graded) or absolute (all-or-none) neural responses in high-level human brain regions is largely unknown. We address this issue with a novel frequency-sweep paradigm probing the evolution of face categorization responses between the minimal and optimal stimulus presentation times. In a first experiment, natural images of variable non-face objects were progressively swept from 120 to 3 ​Hz (8.33–333 ​ms duration) in rapid serial visual presentation sequences. Widely variable face exemplars appeared every 1 ​s, enabling an implicit frequency-tagged face-categorization electroencephalographic (EEG) response at 1 ​Hz. Face-categorization activity emerged with stimulus durations as brief as 17 ​ms (17–83 ​ms across individual participants) but was significant with 33 ​ms durations at the group level. The face categorization response amplitude increased until 83 ​ms stimulus duration (12 ​Hz), implying graded categorization responses. In a second EEG experiment, faces appeared non-periodically throughout such sequences at fixed presentation rates, while participants explicitly categorized faces. A strong correlation between response amplitude and behavioral accuracy across frequency rates suggested that dilution from missed categorizations, rather than a decreased response to each face stimulus, accounted for the graded categorization responses as found in Experiment 1. This was supported by (1) the absence of neural responses to faces that participants failed to categorize explicitly in Experiment 2 and (2) equivalent amplitudes and spatio-temporal signatures of neural responses to behaviorally categorized faces across presentation rates. Overall, these observations provide original evidence that high-level visual categorization of faces, starting at about 100 ​ms following stimulus onset in the human brain, is variable across observers tested under tight temporal constraints, but occurs in an all-or-none fashion.

Putting a name to a face is a highly common activity in our daily life that greatly enriches social interactions. Although this specific person-identity association becomes automatic with learning, it remains difficult and can easily be disrupted in normal circumstances or neurological conditions. To shed light on the neural basis of this important and yet poorly understood association between different input modalities in the human brain, we designed a crossmodal frequency-tagging paradigm coupled to brain activity recording via scalp and intracerebral electroencephalography. In Experiment 1, 12 participants were presented with variable pictures of faces and written names of a single famous identity at a 4-Hz frequency rate while performing an orthogonal task. Every 7 items, another famous identity appeared, either as a face or a name. Robust electrophysiological responses were found exactly at the frequency of identity change (i.e., 4 Hz / 7 = 0.571 Hz), suggesting a crossmodal neural response to person identity. In Experiment 2 with twenty participants, two control conditions with periodic changes of identity for faces or names only were added to estimate the contribution of unimodal neural activity to the putative crossmodal face-name responses. About 30% of the response occurring at the frequency of crossmodal identity change over the left occipito-temporal cortex could not be accounted for by the linear sum of unimodal responses. Finally, intracerebral recordings in the left ventral anterior temporal lobe (ATL) in 7 epileptic patients tested with this paradigm revealed a small number of "pure" crossmodal responses, i.e., with no response to changes of identity for faces or names only. Altogether, these observations provide evidence for integration of verbal and nonverbal person identity-specific information in the human brain, highlighting the contribution of the left ventral ATL in the automatic retrieval of face-name identity associations.

Individuals with autism spectrum disorder (ASD) have difficulties with social communication and interaction. The social motivation hypothesis states that a reduced interest in social stimuli may partly underlie these difficulties. Thus far, however, it has been challenging to quantify individual differences in social orientation and interest, and to pinpoint the neural underpinnings of it. In this study, we tested the neural sensitivity for social versus non-social information in 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ, while children were engaged in an orthogonal task. We recorded electroencephalography (EEG) during fast periodic visual stimulation (FPVS) of social versus non-social stimuli to obtain an objective implicit neural measure of relative social bias. Streams of variable images of faces and houses were superimposed, and each stream of stimuli was tagged with a particular presentation rate (i.e., 6 and 7.5 Hz or vice versa). This frequency-tagging method allows disentangling the respective neural responses evoked by the different streams of stimuli. Moreover, by using superimposed stimuli, we controlled for possible effects of preferential looking, spatial attention, and disengagement. Based on four trials of 60 s, we observed a significant three-way interaction. In the control group, the frequency-tagged neural responses to faces were larger than those to houses, especially in lateral occipito-temporal channels, while the responses to houses were larger over medial occipital channels. In the ASD group, however, faces and houses did not elicit significantly different neural responses in any of the regions. Given the short recording time of the frequency-tagging paradigm with multiple simultaneous inputs and the robustness of the individual responses, the method could be used as a sensitive marker of social preference in a wide range of populations, including younger and challenging populations.

The impact of learning to read in a mixed approach using both the global and phonics teaching methods on the emergence of left hemisphere neural specialization for word recognition is yet unknown in children. Taking advantage of a natural school context with such a mixed approach, we tested 42 first graders behaviorally and with Fast Periodic Visual Stimulation using electroencephalographic recordings (FPVS-EEG) to measure selective neural responses to letter strings. Letter strings were inserted periodically (1/5) in pseudofonts in 40 s sequences displayed at 6 Hz and were either words globally taught at school, that could therefore be processed by visual whole-word form recognition (global method), or control words/pseudowords eliciting grapheme-phoneme (GP) mappings (phonics method). Results show that selective responses (F/5, 1.2 Hz) were left lateralized for control stimuli that triggered GP mappings but bilateral for globally taught words. It implies that neural mechanisms recruited during visual word processing are influenced by the nature of the mapping between written and spoken word forms. GP mappings induce left hemisphere discrimination responses, and visual recognition of whole-word forms induce bilateral responses, probably because the right hemisphere is relatively more involved in holistic visual object recognition. Splitting the group as a function of the mastery of GP mappings into “good” and “poor” readers strongly suggests that good readers actually processed all stimuli (including global words) predominantly with their left hemisphere, while poor readers showed bilateral responses for global words. These results show that in a mixed approach of teaching to read, global method instruction may induce neural processes that differ from those specialized for reading in the left hemisphere. Furthermore, given their difficulties in automatizing GP mappings, poor readers are especially prone to rely on this alternative visual strategy. A preprint of this paper has been released on Biorxiv (van de Walle de Ghelcke et al., 2018).

Abstract This study investigates categorization of human and ape faces in 9-month-olds using a Fast Periodic Visual Stimulation (FPVS) paradigm while measuring EEG. Categorization responses are elicited only if infants discriminate between different categories and generalize across exemplars within each category. In study 1, human or ape faces were presented as standard and deviant stimuli in upright and inverted trials. Upright ape faces presented among humans elicited strong categorization responses, whereas responses for upright human faces and for inverted ape faces were smaller. Deviant inverted human faces did not elicit categorization. Data were best explained by a model with main effects of species and orientation. However, variance of low-level image characteristics was higher for the ape than the human category. Variance was matched to replicate this finding in an independent sample (study 2). Both human and ape faces elicited categorization in upright and inverted conditions, but upright ape faces elicited the strongest responses. Again, data were best explained by a model of two main effects. These experiments demonstrate that 9-month-olds rapidly categorize faces, and unfamiliar faces presented among human faces elicit increased categorization responses. This likely reflects habituation for the familiar standard category, and stronger release for the unfamiliar category deviants.

Abstract The ability to individualize faces is a fundamental human brain function. Following visual adaptation to one individual face, the suppressed neural response to this identity becomes discriminable from an unadapted facial identity at a neural population level. Here, we investigate a simple and objective measure of individual face discrimination with electroencephalographic (EEG) frequency tagging following adaptation. In a first condition, (1) two facial identities are presented in alternation at a rate of six images per second (6 Hz; 3 Hz identity repetition rate) for a 20 s testing sequence, following 10-s adaptation to one of the facial identities; this results in a significant identity discrimination response at 3 Hz in the frequency domain of the EEG over right occipito-temporal channels, replicating our previous findings. Such a 3 Hz response is absent for two novel conditions, in which (2) the faces are inverted and (3) an identity physically equidistant from the two faces is adapted. These results indicate that low-level visual features present in inverted or unspecific facial identities are not sufficient to produce the adaptation effect found for upright facial stimuli, which appears to truly reflect identity-specific perceptual representations in the human brain.

Humans may be the only species able to rapidly and automatically recognize a familiar face identity in a crowd of unfamiliar faces, an important social skill. Here, by combining electroencephalography (EEG) and fast periodic visual stimulation (FPVS), we introduce an ecologically valid, objective and sensitive neural measure of this human individual face recognition function. Natural images of various unfamiliar faces are presented at a fast rate of 6 Hz, allowing one fixation per face, with variable natural images of a highly familiar face identity, a celebrity, appearing every seven images (0.86 Hz). Following a few minutes of stimulation, a high signal-to-noise ratio neural response reflecting the generalized discrimination of the familiar face identity from unfamiliar faces is observed over the occipito-temporal cortex at 0.86 Hz and harmonics. When face images are presented upside-down, the individual familiar face recognition response is negligible, being reduced by a factor of 5 over occipito-temporal regions. Differences in the magnitude of the individual face recognition response across different familiar face identities suggest that factors such as exposure, within-person variability and distinctiveness mediate this response. Our findings of a biological marker for fast and automatic recognition of individual familiar faces with ecological stimuli open an avenue for understanding this function, its development and neural basis in neurotypical individual brains along with its pathology. This should also have implications for the use of facial recognition measures in forensic science.

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. Keywords: Autism, EEG, Face processing

Two areas in the human occipito-temporal cortex respond preferentially to faces: ‘the fusiform face area’ (‘FFA’) and the ‘occipital face area’ (‘OFA’). However, it is unclear whether these areas have an exclusive role in processing faces, or if sub-maximal responses in other visual areas such as the lateral occipital complex (LOC) are also involved. To clarify this issue, we tested a brain-damaged patient (PS) presenting a face-selective impairment with functional magnetic resonance imaging (fMRI). The right hemisphere lesion of the prosoagnosic patient encompasses the ‘OFA’ but preserves the ‘FFA’ and LOC [14,16]. Using fMRI-adaptation, we found a larger response to different faces than repeated faces in the ventral part of the LOC both for normals and the patient, next to her right hemisphere lesion. This observation indicates that following prosopagnosia, areas that do not respond preferentially to faces such as the ventral part of the LOC (vLOC) may still be recruited to subtend residual perception of individual faces.

Human performance at categorizing natural visual images surpasses automatic algorithms, but how and when this function arises and develops remain unanswered. We recorded scalp electrical brain activity in 4–6 months infants viewing images of objects in their natural background at a rapid rate of 6 images/second (6 Hz). Widely variable face images appearing every 5 stimuli generate an electrophysiological response over the right hemisphere exactly at 1.2 Hz (6 Hz/5). This face-selective response is absent for phase-scrambled images and therefore not due to low-level information. These findings indicate that right lateralized face-selective processes emerge well before reading acquisition in the infant brain, which can perform figure-ground segregation and generalize face-selective responses across changes in size, viewpoint, illumination as well as expression, age and gender. These observations made with a highly sensitive and objective approach open an avenue for clarifying the developmental course of natural image categorization in the human brain.

How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (2-tones Mooney figures and Arcimboldo’s facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus (Fusiform face area, FFA) and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no occipital face area, OFA). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient (PS) whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex.

According to an influential view, based on studies of development and of the face inversion effect, human face recognition relies mainly on the treatment of the distances among internal facial features. However, there is surprisingly little evidence supporting this claim. Here, we first use a sample of 515 face photographs to estimate the face recognition information available in interattribute distances. We demonstrate that previous studies of interattribute distances generated faces that exaggerated by 376% this information compared to real-world faces. When human observers are required to recognize faces solely on the basis of real-world interattribute distances, they perform poorly across a broad range of viewing distances (equivalent to 2 to more than 16 m in the real-world). In contrast, recognition is almost perfect when observers recognize faces on the basis of real-world information other than interattribute distances such as attribute shapes and skin properties. We conclude that facial cues other than interattribute distances such as attribute shapes and skin properties are the dominant information of face recognition mechanisms.

Previous studies recording eye movements have rendered inconclusive findings with respect to processing differences between familiar and unfamiliar faces. We argue that this can be attributed to a number of factors that differ across studies: the type and extent of familiarity with stimuli presented, the varying spatial resolution of visual information and/or specifics, the definition of areas of interest subject to analyses, as well as the fact that the time course of scan patterns is often neglected. Here we sought to address these issues by recording gaze patterns in a face recognition task with personally familiar and unfamiliar faces, without predefining areas of interest and investigating potential processing differences at each individual fixation. We found that after a first fixation on the center of mass of the face—suggesting an initial holistic perception—and a subsequent left eye bias, local features were focused and explored more for familiar than unfamiliar faces. Although the number of fixations made did not differ for un-/familiar faces, the locations of fixations began to differ much earlier than when the familiarity decisions were provided. This suggests that without strict time constraints, different types of information are collected relatively early on familiar and unfamiliar faces.

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 5-16 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.

Enhanced N170 ERP responses to both faces and visual words raises questions about category specific processing mechanisms during early perception and their neural basis. Topographic differences across word and face N170s might suggest a form of category specific processing in early perception - the word N170 is consistently left lateralized, while less consistent evidence suggests a right lateralization for the face N170. Additionally, the face N170 shows a reduction in amplitude across consecutive unique faces, a form of habituation that might differ across studies thereby helping to explain inconsistencies in lateralization. This effect remains unexplored for visual words. The current study directly contrasts N170 responses to words and faces within the same subjects, examining both category-level habituation and lateralization effects. ERP responses to a series of different faces and words were collected under two contexts: blocks that alternated faces and words versus pure blocks designed to induce category level habituation. Global and occipito-temporal measures of N170 amplitude demonstrated an interaction between category (word, faces) and block context (alternating, pure). N170 amplitude demonstrated class level habituation for faces but not words. Furthermore, the pure block context diminished the right lateralization of the face N170, potentially pointing to class level habituation as a factor that might drive inconsistencies of right lateralization across different paradigms. No analogous effect for the word N170 was found, suggesting category specificity for this process. Taken together, these topographic and habituation effects suggest distinct forms of perceptual processing drive the face N170 and the visual word form N170.

BACKGROUND: Using the well-known composite illusion as a marker of the holistic perception of faces, we tested how prolonged visual experience with a specific population of faces (4- to 6-year-old children) modulates the face perception system in adulthood. METHODOLOGY/PRINCIPAL FINDINGS: We report a face composite effect that is larger for adult than children faces in a group of adults without experience with children faces ("children-face novices"), while it is of equal magnitude for adults and children faces in a population of preschool teachers ("children-face experts"). When considering preschool teachers only, we observed a significant correlation between the number of years of experience with children faces and the differential face composite effect between children and adults faces. Participants with at least 10 years of qualitative experience with children faces had a larger composite face effect for children than adult faces. CONCLUSIONS/SIGNIFICANCE: Overall, these observations indicate that even in adulthood face processes can be reshaped qualitatively, presumably to facilitate efficient processing of the differential morphological features of the frequently encountered population of faces.