Visual periodicity reveals distinct attentional signatures for face and non-face categories.

Observers can selectively deploy attention to regions of space, moments in time, specific visual features, individual objects, and even specific high-level categories-for example, when keeping an eye out for dogs while jogging. Here, we exploited visual periodicity to examine how category-based attention differentially modulates selective neural processing of face and non-face categories. We combined electroencephalography with a novel frequency-tagging paradigm capable of capturing selective neural responses for multiple visual categories contained within the same rapid image stream (faces/birds in Exp 1; houses/birds in Exp 2). We found that the pattern of attentional enhancement and suppression for face-selective processing is unique compared to other object categories: Where attending to non-face objects strongly enhances their selective neural signals during a later stage of processing (300-500 ms), attentional enhancement of face-selective processing is both earlier and comparatively more modest. Moreover, only the selective neural response for faces appears to be actively suppressed by attending towards an alternate visual category. These results underscore the special status that faces hold within the human visual system, and highlight the utility of visual periodicity as a powerful tool for indexing selective neural processing of multiple visual categories contained within the same image sequence.

The power of rhythms: how steady-state evoked responses reveal early neurocognitive development.

Electroencephalography (EEG) is a non-invasive and painless recording of cerebral activity, particularly well-suited for studying young infants, allowing the inspection of cerebral responses in a constellation of different ways. Of particular interest for developmental cognitive neuroscientists is the use of rhythmic stimulation, and the analysis of steady-state evoked potentials (SS-EPs) - an approach also known as frequency tagging. In this paper we rely on the existing SS-EP early developmental literature to illustrate the important advantages of SS-EPs for studying the developing brain. We argue that (1) the technique is both objective and predictive: the response is expected at the stimulation frequency (and/or higher harmonics), (2) its high spectral specificity makes the computed responses particularly robust to artifacts, and (3) the technique allows for short and efficient recordings, compatible with infants' limited attentional spans. We additionally provide an overview of some recent inspiring use of the SS-EP technique in adult research, in order to argue that (4) the SS-EP approach can be implemented creatively to target a wide range of cognitive and neural processes. For all these reasons, we expect SS-EPs to play an increasing role in the understanding of early cognitive processes. Finally, we provide practical guidelines for implementing and analyzing SS-EP studies.

Reduced adaptability, but no fundamental disruption, of norm-based face coding following early visual deprivation from congenital cataracts.

Faces are adaptively coded relative to visual norms that are updated by experience, and this adaptive coding is linked to face recognition ability. Here we investigated whether adaptive coding of faces is disrupted in individuals (adolescents and adults) who experience face recognition difficulties following visual deprivation from congenital cataracts in infancy. We measured adaptive coding using face identity aftereffects, where smaller aftereffects indicate less adaptive updating of face-coding mechanisms by experience. We also examined whether the aftereffects increase with adaptor identity strength, consistent with norm-based coding of identity, as in typical populations, or whether they show a different pattern indicating some more fundamental disruption of face-coding mechanisms. Cataract-reversal patients showed significantly smaller face identity aftereffects than did controls (Experiments 1 and 2). However, their aftereffects increased significantly with adaptor strength, consistent with norm-based coding (Experiment 2). Thus we found reduced adaptability but no fundamental disruption of norm-based face-coding mechanisms in cataract-reversal patients. Our results suggest that early visual experience is important for the normal development of adaptive face-coding mechanisms.

Three-month-old infants' sensitivity to horizontal information within faces.

Horizontal information is crucial to face processing in adults. Yet the ontogeny of this preferential type of processing remains unknown. To clarify this issue, we tested 3-month-old infants' sensitivity to horizontal information within faces. Specifically, infants were exposed to the simultaneous presentation of a face and a car presented in upright or inverted orientation while their looking behavior was recorded. Face and car images were either broadband (UNF) or filtered to only reveal horizontal (H), vertical (V) or this combined information (HV). As expected, infants looked longer at upright faces than at upright cars, but critically, only when horizontal information was preserved in the stimulus (UNF, HV, H). These results first indicate that horizontal information already drives upright face processing at 3 months of age. They also recall the importance, for infants, of some facial features, arranged in a top-heavy configuration, particularly revealed by this band of information. © 2016 Wiley Periodicals, Inc. Dev Psychobiol 58: 536-542, 2016.

Face memory deficits in patients deprived of early visual input by bilateral congenital cataracts.

Patients treated for bilateral congenital cataract are later impaired on several hallmarks of adults' expertise with upright faces but report no problem with remembering faces. Here, we provide the first formal data on their face memory. We compared 12 adults with a history of visual deprivation from bilateral congenital cataracts to 24 age-matched controls with normal vision on their ability to recognize famous and recently learned faces, and on their subjective impression of their face memory. Bilateral congenital cataract patients demonstrated a prosopagnosic-like deficit, being slower and less accurate in recognizing both famous faces and recently learned faces, despite not differing on most questions about their impression of their face memory. Patients' results on three perceptual tasks (the composite face effect, the Benton test of recognizing faces through a change in point of view, and the Jane test of sensitivity to feature spacing) were also not correlated with their face memory deficits. These results suggest that early visual input is necessary not only for perceptual expertise in differentiating among unfamiliar upright faces, but also for normal accuracy in remembering the identity of individual faces.

What determines the neural response to snakes in the infant brain? A systematic comparison of color and grayscale stimuli.

Snakes and primates have coexisted for thousands of years. Given that snakes are the first of the major primate predators, natural selection may have favored primates whose snake detection abilities allowed for better defensive behavior. Aligning with this idea, we recently provided evidence for an inborn mechanism anchored in the human brain that promptly detects snakes, based on their characteristic visual features. What are the critical visual features driving human neural responses to snakes is an unresolved issue. While their prototypical curvilinear coiled shape seems of major importance, it remains possible that the brain responds to a blend of other visual features. Coloration, in particular, might be of major importance, as it has been shown to act as a powerful aposematic signal. Here, we specifically examine whether color impacts snake-specific responses in the naive, immature infant brain. For this purpose, we recorded the brain activity of 6-to 11-month-old infants using electroencephalography (EEG), while they watched sequences of color or grayscale animal pictures flickering at a periodic rate. We showed that glancing at colored and grayscale snakes generated specific neural responses in the occipital region of the brain. Color did not exert a major influence on the infant brain response but strongly increased the attention devoted to the visual streams. Remarkably, age predicted the strength of the snake-specific response. These results highlight that the expression of the brain-anchored reaction to coiled snakes bears on the refinement of the visual system.

The role of experience during childhood in shaping the other-race effect.

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

Learning to Be Conscious.

Consciousness remains a formidable challenge. Different theories of consciousness have proposed vastly different mechanisms to account for phenomenal experience. Here, appealing to aspects of global workspace theory, higher-order theories, social theories, and predictive processing, we introduce a novel framework: the self-organizing metarerpresentational account (SOMA), in which consciousness is viewed as something that the brain learns to do. By this account, the brain continuously and unconsciously learns to redescribe its own activity to itself, so developing systems of metarepresentations that qualify target first-order representations. Thus, experiences only occur in experiencers that have learned to know they possess certain first-order states and that have learned to care more about certain states than about others. In this sense, consciousness is the brain's (unconscious, embodied, enactive, nonconceptual) theory about itself.

Unconscious categorization of sub-millisecond complex images.

Can people categorize complex visual scenes unconsciously? The possibility of unconscious perception remains controversial. Here, we addressed this question using psychophysical methods applied to unmasked visual stimuli presented for extremely short durations (in the µsec range) by means of a custom-built modern tachistoscope. Our experiment was composed of two phases. In the first phase, natural or urban scenes were either absent or present (for varying durations) on the tachistoscope screen, and participants were simply asked to evaluate their subjective perception using a 3-points scale (absence of stimulus, stimulus detection or stimulus identification). Participants' responses were tracked by means of two staircases. The first psychometric function aimed at defining participants' proportion of subjective detection responses (i.e., not having seen anything vs. having seen something without being able to identify it), while the second staircase tracked the proportion of subjective identification rates (i.e., being unaware of the stimulus' category vs. being aware of it). In the second phase, the same participants performed an objective categorization task in which they had to decide, on each trial, whether the image was a natural vs. an urban scene. A third staircase was used in this phase so as to build a psychometric curve reflecting the objective categorization performance of each participant. In this second phase, participants also rated their subjective perception of each stimulus on every trial, exactly as in the first phase of the experiment. Our main result is that objective categorization performance, here assumed to reflect the contribution of both conscious and unconscious trials, cannot be explained based exclusively on conscious trials. This clearly suggests that the categorization of complex visual scenes is possible even when participants report being unable to consciously perceive the contents of the stimulus.

Braille readers break mirror invariance for both visual Braille and Latin letters.

For this study, we started from the observation that the poor adequacy of a script to the requirements of the human visual system strongly impacts some aspects of reading expertise (e.g., fluent reading). Here we investigated another of these aspects, namely the ability to break mirror invariance, which makes it hard for readers to ignore the mirrored contrasts of letters even if this hinders performance. In particular, we hypothesized that this ability would be preserved for the visually presented letters of the Braille alphabet despite their poor fit to the constraints of the human visual system, as it did for congenital Braille readers when they explored the same letters through the tactile modality (de Heering, Collignon, & Kolinsky, 2018). To test so, we measured visual Braille readers' mirror costs, indexing for their difficulty to consider mirrored items as identical compared to strictly identical items, for three materials: Braille letters, geometrical shapes and Latin letters, which invariant properties are typically considered as having been selected through cultural evolution because they match the requirements of the visual system. Contrary to people having never experienced Braille, Braille readers' mirror cost was of the same magnitude for Latin letters and Braille letters and steadily increased the more they had experience with the latter material. Both these costs were also stronger than what was observed for geometrical shapes. Overall these results suggest that the poor adequacy of the Braille alphabet to the visual system does not impede Braille readers to break mirror invariance for the Braille material.

The non-linear development of the right hemispheric specialization for human face perception.

The developmental origins of human adults' right hemispheric specialization for face perception remain unclear. On the one hand, infant studies have shown a right hemispheric advantage for face perception. On the other hand, it has been proposed that the adult right hemispheric lateralization for face perception slowly emerges during childhood due to reading acquisition, which increases left lateralized posterior responses to competing written material (e.g., visual letters and words). Since methodological approaches used in infant and children typically differ when their face capabilities are explored, resolving this issue has been difficult. Here we tested 5-year-old preschoolers varying in their level of visual letter knowledge with the same fast periodic visual stimulation (FPVS) paradigm leading to strongly right lateralized electrophysiological occipito-temporal face-selective responses in 4- to 6-month-old infants (de Heering and Rossion, 2015). Children's face-selective response was quantitatively larger and differed in scalp topography from infants', but did not differ across hemispheres. There was a small positive correlation between preschoolers' letter knowledge and a non-normalized index of right hemispheric specialization for faces. These observations show that previous discrepant results in the literature reflect a genuine nonlinear development of the neural processes underlying face perception and are not merely due to methodological differences across age groups. We discuss several factors that could contribute to the adult right hemispheric lateralization for faces, such as myelination of the corpus callosum and reading acquisition. Our findings point to the value of FPVS coupled with electroencephalography to assess specialized face perception processes throughout development with the same methodology.

Newborns' face recognition is based on spatial frequencies below 0.5 cycles per degree.

A critical question in Cognitive Science concerns how knowledge of specific domains emerges during development. Here we examined how limitations of the visual system during the first days of life may shape subsequent development of face processing abilities. By manipulating the bands of spatial frequencies of face images, we investigated what is the nature of the visual information that newborn infants rely on to perform face recognition. Newborns were able to extract from a face the visual information lying from 0 to 1 cpd (Experiment 1), but only a narrower 0-0.5 cpd spatial frequency range was successful to accomplish face recognition (Experiment 2). These results provide the first empirical support of a low spatial frequency advantage in individual face recognition at birth and suggest that early in life low-level, non-specific perceptual constraints affect the development of the face processing system.

Blind readers break mirror invariance as sighted do.

Mirror invariance refers to a predisposition of humans, including infants and animals, which urge them to consider mirrored images as corresponding to the same object. Yet in order to learn to read a written system that incorporates mirrored letters (e.g., vs. in the Latin alphabet), humans learn to break this perceptual bias. Here we examined the role visual experience and input modality play in the emergence of this bias. To this end, we tested congenital blind (CB) participants in two same-different tactile comparison tasks including pairs of mirrored and non-mirrored Braille letters as well as embossed unfamiliar geometric shapes and Latin letters, and compared their results to those of age-matched sighted participants involved in similar but visually-presented tasks. Sighted participants showed a classical pattern of results for their material of expertise, Latin letters. CB's results signed for their expertise with the Braille script compared to the other two materials that they processed according to an internal frame of reference. They also evidenced that they automatically break mirror invariance for different materials explored through the tactile modality, including Braille letters. Altogether, these results demonstrate that learning to read Braille through the tactile modality allows breaking mirror invariance in a comparable way to what is observed in sighted individuals for the mirrored letters of the Latin alphabet.

Is Red Heavier Than Yellow Even for Blind?

Across cultures and languages, people find similarities between the products of different senses in mysterious ways. By studying what is called cross-modal correspondences, cognitive psychologists discovered that lemons are fast rather than slow, boulders are sour, and red is heavier than yellow. Are these cross-modal correspondences established via sensory perception or can they be learned merely through language? We contribute to this debate by demonstrating that early blind people who lack the perceptual experience of color also think that red is heavier than yellow but to a lesser extent than sighted do.

A Brief Period of Postnatal Visual Deprivation Alters the Balance between Auditory and Visual Attention.

Is a short and transient period of visual deprivation early in life sufficient to induce lifelong changes in how we attend to, and integrate, simple visual and auditory information [1, 2]? This question is of crucial importance given the recent demonstration in both animals and humans that a period of blindness early in life permanently affects the brain networks dedicated to visual, auditory, and multisensory processing [1-16]. To address this issue, we compared a group of adults who had been treated for congenital bilateral cataracts during early infancy with a group of normally sighted controls on a task requiring simple detection of lateralized visual and auditory targets, presented alone or in combination. Redundancy gains obtained from the audiovisual conditions were similar between groups and surpassed the reaction time distribution predicted by Miller's race model. However, in comparison to controls, cataract-reversal patients were faster at processing simple auditory targets and showed differences in how they shifted attention across modalities. Specifically, they were faster at switching attention from visual to auditory inputs than in the reverse situation, while an opposite pattern was observed for controls. Overall, these results reveal that the absence of visual input during the first months of life does not prevent the development of audiovisual integration but enhances the salience of simple auditory inputs, leading to a different crossmodal distribution of attentional resources between auditory and visual stimuli.

Rapid categorization of natural face images in the infant right hemisphere.

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.

Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation.

Animal and human studies have demonstrated that transient visual deprivation early in life, even for a very short period, permanently alters the response properties of neurons in the visual cortex and leads to corresponding behavioral visual deficits. While it is acknowledged that early-onset and longstanding blindness leads the occipital cortex to respond to non-visual stimulation, it remains unknown whether a short and transient period of postnatal visual deprivation is sufficient to trigger crossmodal reorganization that persists after years of visual experience. In the present study, we characterized brain responses to auditory stimuli in 11 adults who had been deprived of all patterned vision at birth by congenital cataracts in both eyes until they were treated at 9 to 238 days of age. When compared to controls with typical visual experience, the cataract-reversal group showed enhanced auditory-driven activity in focal visual regions. A combination of dynamic causal modeling with Bayesian model selection indicated that this auditory-driven activity in the occipital cortex was better explained by direct cortico-cortical connections with the primary auditory cortex than by subcortical connections. Thus, a short and transient period of visual deprivation early in life leads to enduring large-scale crossmodal reorganization of the brain circuitry typically dedicated to vision.

The effect of spatial frequency on perceptual learning of inverted faces.

We investigated the efficacy of training adults to recognize full spectrum inverted faces presented with different viewpoints. To examine the role of different spatial frequencies in any learning, we also used high-pass filtered faces that preserved featural information and low-pass filtered faces that severely reduced that featural information. Although all groups got faster over the 2 days of training, there was more improvement in accuracy for the group exposed to full spectrum faces than in the two groups exposed to filtered faces, both of which improved more modestly and only when the same faces were shown on the 2 days of training. For the group exposed to the full spectrum range and, to a lesser extent, for those exposed to high frequency faces, training generalized to a new set of full spectrum faces of a different size in a different task, but did not lead to evidence of holistic processing or improved sensitivity to feature shape or spacing in inverted faces. Overall these results demonstrate that only 2h of practice in recognizing full-spectrum inverted faces presented from multiple points of view is sufficient to improve recognition of the trained faces and to generalize to novel instances. Perceptual learning also occurred for low and high frequency faces but to a smaller extent.

The composite-face effect survives asymmetric face distortions.

In two experiments, we investigated whether adults use holistic processing even for faces that are grossly distorted because their eyes have been moved asymmetrically to violate the common layout of a face (distorting its first-order relations). To this end we used a compelling demonstration that faces are processed as wholes, the composite-face effect. Specifically, adults judged the similarity of sequentially presented top halves of normal (original condition) and distorted faces with one eye (one-eye condition) or two eyes (two-eyes condition) shifted up by an abnormal amount. Trials were either blocked by type of distortion (experiment 1) or intermixed within the experiment (experiment 2). In both experiments, participants demonstrated a composite-face effect of the same magnitude in the three conditions, a pattern suggesting that they processed holistically even faces whose first-order relations were violated.