Olfactory-to-visual facilitation in the infant brain declines gradually from 4 to 12 months.

During infancy, intersensory facilitation declines gradually as unisensory perception develops. However, this trade-off was mainly investigated using audiovisual stimulations. Here, fifty 4- to 12-month-old infants (26 females, predominately White) were tested in 2017-2020 to determine whether the facilitating effect of their mother's body odor on neural face categorization, as previously observed at 4 months, decreases with age. In a baseline odor context, the results revealed a face-selective electroencephalographic response that increases and changes qualitatively between 4 and 12 months, marking improved face categorization. At the same time, the benefit of adding maternal odor fades with age (R2 = .31), indicating an inverse relation with the amplitude of the visual response, and generalizing to olfactory-visual interactions previous evidence from the audiovisual domain.

Odor-driven face-like categorization in the human infant brain.

Understanding how the young infant brain starts to categorize the flurry of ambiguous sensory inputs coming in from its complex environment is of primary scientific interest. Here, we test the hypothesis that senses other than vision play a key role in initiating complex visual categorizations in 20 4-mo-old infants exposed either to a baseline odor or to their mother's odor while their electroencephalogram (EEG) is recorded. Various natural images of objects are presented at a 6-Hz rate (six images/second), with face-like object configurations of the same object categories (i.e., eliciting face pareidolia in adults) interleaved every sixth stimulus (i.e., 1 Hz). In the baseline odor context, a weak neural categorization response to face-like stimuli appears at 1 Hz in the EEG frequency spectrum over bilateral occipitotemporal regions. Critically, this face-like-selective response is magnified and becomes right lateralized in the presence of maternal body odor. This reveals that nonvisual cues systematically associated with human faces in the infant's experience shape the interpretation of face-like configurations as faces in the right hemisphere, dominant for face categorization. At the individual level, this intersensory influence is particularly effective when there is no trace of face-like categorization in the baseline odor context. These observations provide evidence for the early tuning of face-(like)-selective activity from multisensory inputs in the developing brain, suggesting that perceptual development integrates information across the senses for efficient category acquisition, with early maturing systems such as olfaction driving the acquisition of categories in later-developing systems such as vision.

Towards an optimization of functional localizers in non-human primate neuroimaging with (fMRI) frequency-tagging.

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.

Neurophysiological evidence for crossmodal (face-name) person-identity representation in the human left ventral temporal cortex.

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.

Automatic, Early Color-Specific Neural Responses to Object Color Knowledge.

Some familiar objects are associated with specific colors, e.g., rubber ducks with yellow. Whether and at what stage neural responses occur to these color associations remain open questions. We recorded frequency-tagged electroencephalogram (EEG) responses to periodic presentations of yellow-associated objects, shown among sequences of non-periodic blue-, red-, and green-associated objects. Both color and grayscale versions of the objects elicited yellow-specific responses, indicating an automatic activation of color knowledge from object shape. Follow-up experiments replicated these effects with green-specific responses, and demonstrated modulated responses for incongruent color/object associations. Importantly, the onset of color-specific responses was as early to grayscale as actually colored stimuli (before 100 ms), the latter additionally eliciting a conventional later response (approximately 140-230 ms) to actual stimulus color. This suggests that the neural representation of familiar objects includes both diagnostic shape and color properties, such that shape can elicit associated color-specific responses before actual color-specific responses occur.

Coarse-to-Fine(r) Automatic Familiar Face Recognition in the Human Brain.

At what level of spatial resolution can the human brain recognize a familiar face in a crowd of strangers? Does it depend on whether one approaches or rather moves back from the crowd? To answer these questions, 16 observers viewed different unsegmented images of unfamiliar faces alternating at 6 Hz, with spatial frequency (SF) content progressively increasing (i.e., coarse-to-fine) or decreasing (fine-to-coarse) in different sequences. Variable natural images of celebrity faces every sixth stimulus generated an objective neural index of single-glanced automatic familiar face recognition (FFR) at 1 Hz in participants' electroencephalogram (EEG). For blurry images increasing in spatial resolution, the neural FFR response over occipitotemporal regions emerged abruptly with additional cues at about 6.3-8.7 cycles/head width, immediately reaching amplitude saturation. When the same images progressively decreased in resolution, the FFR response disappeared already below 12 cycles/head width, thus providing no support for a predictive coding hypothesis. Overall, these observations indicate that rapid automatic recognition of heterogenous natural views of familiar faces is achieved from coarser visual inputs than generally thought, and support a coarse-to-fine FFR dynamics in the human brain.

A genuine interindividual variability in number and anatomical localization of face-selective regions in the human brain.

Neuroimaging studies have reported regions with more neural activation to face than nonface stimuli in the human occipitotemporal cortex for three decades. Here we used a highly sensitive and reliable frequency-tagging functional magnetic resonance imaging paradigm measuring high-level face-selective neural activity to assess interindividual variability in the localization and number of face-selective clusters. Although the majority of these clusters are located in the same cortical gyri and sulci across 25 adult brains, a volume-based analysis of unsmoothed data reveals a large amount of interindividual variability in their spatial distribution and number, particularly in the ventral occipitotemporal cortex. In contrast to the widely held assumption, these face-selective clusters cannot be objectively related on a one-to-one basis across individual brains, do not correspond to a single cytoarchitectonic region, and are not clearly demarcated by estimated posteroanterior cytoarchitectonic borders. Interindividual variability in localization and number of cortical face-selective clusters does not appear to be due to the measurement noise but seems to be genuine, casting doubt on definite labeling and interindividual correspondence of face-selective "areas" and questioning their a priori definition based on cytoarchitectony or probabilistic atlases of independent datasets. These observations challenge conventional models of human face recognition based on a fixed number of discrete neurofunctional information processing stages.

EEG Frequency Tagging Reveals the Integration of Form and Motion Cues into the Perception of Group Movement.

The human brain has dedicated mechanisms for processing other people's movements. Previous research has revealed how these mechanisms contribute to perceiving the movements of individuals but has left open how we perceive groups of people moving together. Across three experiments, we test whether movement perception depends on the spatiotemporal relationships among the movements of multiple agents. In Experiment 1, we combine EEG frequency tagging with apparent human motion and show that posture and movement perception can be dissociated at harmonically related frequencies of stimulus presentation. We then show that movement but not posture processing is enhanced when observing multiple agents move in synchrony. Movement processing was strongest for fluently moving synchronous groups (Experiment 2) and was perturbed by inversion (Experiment 3). Our findings suggest that processing group movement relies on binding body postures into movements and individual movements into groups. Enhanced perceptual processing of movement synchrony may form the basis for higher order social phenomena such as group alignment and its social consequences.

Intracerebral electrical stimulation of the right anterior fusiform gyrus impairs human face identity recognition.

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.

Developmental experiences alter the temporal processing characteristics of the visual cortex: Evidence from deaf and hearing native signers.

To date, the extent to which early experience shapes the functional characteristics of neural circuits is still a matter of debate. In the present study, we tested whether congenital deafness and/or the acquisition of a sign language alter the temporal processing characteristics of the visual system. Moreover, we investigated whether, assuming cross-modal plasticity in deaf individuals, the temporal processing characteristics of possibly reorganised auditory areas resemble those of the visual cortex. Steady-state visual evoked potentials (SSVEPs) were recorded in congenitally deaf native signers, hearing native signers, and hearing nonsigners. The luminance of the visual stimuli was periodically modulated at 12, 21, and 40 Hz. For hearing nonsigners, the optimal driving rate was 12 Hz. By contrast, for the group of hearing signers, the optimal driving rate was 12 and 21 Hz, whereas for the group of deaf signers, the optimal driving rate was 21 Hz. We did not observe evidence for cross-modal recruitment of auditory cortex in the group of deaf signers. These results suggest a higher preferred neural processing rate as a consequence of the acquisition of a sign language.

Harmonic Amplitude Summation for Frequency-tagging Analysis.

In the approach of frequency tagging, stimuli that are presented periodically generate periodic responses of the brain. Following a transformation into the frequency domain, the brain's response is often evident at the frequency of stimulation, F, and its higher harmonics (2F, 3F, etc.). This approach is increasingly used in neuroscience, as it affords objective measures to characterize brain function. However, whether these specific harmonic frequency responses should be combined for analysis-and if so, how-remains an outstanding issue. In most studies, higher harmonic responses have not been described or were described only individually; in other studies, harmonics have been combined with various approaches, for example, averaging and root-mean-square summation. A rationale for these approaches in the context of frequency-based analysis principles and an understanding of how they relate to the brain's response amplitudes in the time domain have been missing. Here, with these elements addressed, the summation of (baseline-corrected) harmonic amplitude is recommended.

Critical information thresholds underlying generic and familiar face categorisation at the same face encounter.

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.

Implicit, automatic semantic word categorisation in the left occipito-temporal cortex as revealed by fast periodic visual stimulation.

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.

Intracerebral electrical stimulation to understand the neural basis of human face identity recognition.

Recognizing people's identity by their faces is a key function in the human species, supported by regions of the ventral occipito-temporal cortex (VOTC). In the last decade, there have been several reports of perceptual face distortion during direct electrical stimulation (DES) with subdural electrodes positioned over a well-known face-selective VOTC region of the right lateral middle fusiform gyrus (LatMidFG; i.e., the "Fusiform Face Area", FFA). However, transient impairments of face identity recognition (FIR) have been extremely rare and only behaviorally quantified during DES with intracerebral (i.e., depth) electrodes in stereo-electroencephalography (SEEG). The three detailed cases reported so far, summarized here, were specifically impaired at FIR during DES inside different anatomical VOTC regions of the right hemisphere: the inferior occipital gyrus (IOG) and the LatMidFG, as well as a region that lies at the heart of a large magnetic susceptibility artifact in functional magnetic resonance imaging (fMRI): the anterior fusiform gyrus (AntFG). In the first two regions, the eloquent electrode contacts were systematically associated with the highest face-selective and (unfamiliar) face individuation responses as measured with intracerebral electrophysiology. Stimulation in the right AntFG did not lead to perceptual changes but also caused an inability to remember having been presented face pictures, as if the episode was never recorded in memory. These observations support the view of an extensive network of face-selective VOTC regions subtending human FIR, with at least three critical nodes in the right hemisphere associated with differential intrinsic and extrinsic patterns of reentrant connectivity.

Developmental changes in neural letter-selectivity: A 1-year follow-up of beginning readers.

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.

Spatially Dissociated Intracerebral Maps for Face- and House-Selective Activity in the Human Ventral Occipito-Temporal Cortex.

We report a comprehensive mapping of the human ventral occipito-temporal cortex (VOTC) for selective responses to frequency-tagged faces or landmarks (houses) presented in rapid periodic trains of objects, with intracerebral recordings in a large sample (N = 75). Face-selective contacts are three times more numerous than house-selective contacts and show a larger amplitude, with a right hemisphere advantage for faces. Most importantly, these category-selective contacts are spatially dissociated along the lateral-to-medial VOTC axis, respectively, consistent with neuroimaging evidence. At the minority of "overlap" contacts responding selectively to both faces and houses, response amplitude to the two categories is not correlated, suggesting a contribution of distinct populations of neurons responding selectively to each category. The medio-lateral dissociation also extends into the underexplored anterior temporal lobe (ATL). In this region, a relatively high number of intracerebral recording contacts show category-exclusive responses (i.e., without any response to baseline visual objects) to faces but rarely to houses, in line with the proposed role of this region in processing people-related semantic information. Altogether, these observations shed novel insight on the neural basis of human visual recognition and strengthen the validity of the frequency-tagging approach coupled with intracerebral recordings in epileptic patients to understand human brain function.

Selective visual representation of letters and words in the left ventral occipito-temporal cortex with intracerebral recordings.

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.

All-or-none face categorization in the human brain.

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 â€‹Hz (8.33-333 â€‹ms duration) in rapid serial visual presentation sequences. Widely variable face exemplars appeared every 1 â€‹s, enabling an implicit frequency-tagged face-categorization electroencephalographic (EEG) response at 1 â€‹Hz. Face-categorization activity emerged with stimulus durations as brief as 17 â€‹ms (17-83 â€‹ms across individual participants) but was significant with 33 â€‹ms durations at the group level. The face categorization response amplitude increased until 83 â€‹ms stimulus duration (12 â€‹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 â€‹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.

The neural basis of rapid unfamiliar face individuation with human intracerebral recordings.

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.

EEG frequency-tagging demonstrates increased left hemispheric involvement and crossmodal plasticity for face processing in congenitally deaf signers.

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.