Backward masking reveals coarse-to-fine dynamics in human V1.

Natural images exhibit luminance variations aligned across a broad spectrum of spatial frequencies (SFs). It has been proposed that, at early stages of processing, the coarse signals carried by the low SF (LSF) of the visual input are sent rapidly from primary visual cortex (V1) to ventral, dorsal and frontal regions to form a coarse representation of the input, which is later sent back to V1 to guide the processing of fine-grained high SFs (i.e., HSF). We used functional resonance imaging (fMRI) to investigate the role of human V1 in the coarse-to-fine integration of visual input. We disrupted the processing of the coarse and fine content of full-spectrum human face stimuli via backward masking of selective SF ranges (LSFs: <1.75cpd and HSFs: >1.75cpd) at specific times (50, 83, 100 or 150 ms). In line with coarse-to-fine proposals, we found that (1) the selective masking of stimulus LSF disrupted V1 activity in the earliest time window, and progressively decreased in influence, while (2) an opposite trend was observed for the masking of stimulus' HSF. This pattern of activity was found in V1, as well as in ventral (i.e. the Fusiform Face area, FFA), dorsal and orbitofrontal regions. We additionally presented subjects with contrast negated stimuli. While contrast negation significantly reduced response amplitudes in the FFA, as well as coupling between FFA and V1, coarse-to-fine dynamics were not affected by this manipulation. The fact that V1 response dynamics to strictly identical stimulus sets differed depending on the masked scale adds to growing evidence that V1 role goes beyond the early and quasi-passive transmission of visual information to the rest of the brain. It instead indicates that V1 may yield a 'spatially registered common forum' or 'blackboard' that integrates top-down inferences with incoming visual signals through its recurrent interaction with high-level regions located in the inferotemporal, dorsal and frontal regions.

Radial bias in face identification.

Human vision in the periphery is most accurate for stimuli that point towards the fovea. This so-called radial bias has been linked with the organization and spatial selectivity of neurons at the lowest levels of the visual system, from retinal ganglion cells onwards. Despite evidence that the human visual system is radially biased, it is not yet known whether this bias persists at higher levels of processing, or whether high-level representations are invariant to this low-level orientation bias. We used the case of face identity recognition to address this question. The specialized high-level mechanisms that support efficient face recognition are highly dependent on horizontally oriented information, which convey the most useful identity cues in the fovea. We show that face selective mechanisms are more sensitive on the horizontal meridian (to the left and right of fixation) compared to the vertical meridian (above and below fixation), suggesting that the horizontal cues in the face are better extracted on the horizontal meridian, where they align with the radial bias. The results demonstrate that the radial bias is maintained at high-level recognition stages and emphasize the importance of accounting for the radial bias in future investigation of visual recognition processes in peripheral vision.

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.

Information redundancy across spatial scales modulates early visual cortical processing.

Visual images contain redundant information across spatial scales where low spatial frequency contrast is informative towards the location and likely content of high spatial frequency detail. Previous research suggests that the visual system makes use of those redundancies to facilitate efficient processing. In this framework, a fast, initial analysis of low-spatial frequency (LSF) information guides the slower and later processing of high spatial frequency (HSF) detail. Here, we used multivariate classification as well as time-frequency analysis of MEG responses to the viewing of intact and phase scrambled images of human faces to demonstrate that the availability of redundant LSF information, as found in broadband intact images, correlates with a reduction in HSF representational dominance in both early and higher-level visual areas as well as a reduction of gamma-band power in early visual cortex. Our results indicate that the cross spatial frequency information redundancy that can be found in all natural images might be a driving factor in the efficient integration of fine image details.

Coarse-to-fine information integration in human vision.

Coarse-to-fine theories of vision propose that the coarse information carried by the low spatial frequencies (LSF) of visual input guides the integration of finer, high spatial frequency (HSF) detail. Whether and how LSF modulates HSF processing in naturalistic broad-band stimuli is still unclear. Here we used multivariate decoding of EEG signals to separate the respective contribution of LSF and HSF to the neural response evoked by broad-band images. Participants viewed images of human faces, monkey faces and phase-scrambled versions that were either broad-band or filtered to contain LSF or HSF. We trained classifiers on EEG scalp-patterns evoked by filtered scrambled stimuli and evaluated the derived models on broad-band scrambled and intact trials. We found reduced HSF contribution when LSF was informative towards image content, indicating that coarse information does guide the processing of fine detail, in line with coarse-to-fine theories. We discuss the potential cortical mechanisms underlying such coarse-to-fine feedback.

Ultra-coarse, single-glance human face detection in a dynamic visual stream.

Effective human interaction depends on our ability to rapidly detect faces in dynamic visual environments. Here we asked how basic units of visual information (spatial frequencies, or SF) contribute to this fundamental brain function. Human observers viewed initially blurry, unrecognizable natural object images presented at a fast 12 Hz rate and parametrically increasing in SF content over the course of 1 minute. By inserting highly variable natural face images as every 8th stimulus, we captured an objective neural index of face detection in participants' electroencephalogram (EEG) at exactly 1.5 Hz. This face-selective signal emerged over the right occipito-temporal cortex at <5 cycles/image, suggesting that the brain can - at a single glance - discriminate vastly different faces from multiple unsegmented object categories using only very coarse visual information. Local features (e.g., eyes) are not yet discernable at this threshold, indicating that fast face detection critically relies on global facial configuration. Interestingly, the face-selective neural response continued to increase with additional higher SF content until saturation around >50 cycles/image, potentially supporting higher-level recognition functions (e.g., facial identity recognition).

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.

Brain Activation Associated with Automatic Processing of Alcohol-Related Cues in Young Heavy Drinkers and Its Modulation by Alcohol Administration.

BACKGROUND: While the automatic processing of alcohol-related cues by alcohol abusers is well established in experimental psychopathology approaches, the cerebral regions involved in this phenomenon and the influence of alcohol intake on this process remain unknown. The aim of this functional magnetic resonance imaging (fMRI) study was to investigate the neural mechanisms underlying the processing of task-irrelevant alcohol-related stimuli in young heavy drinkers and their modulation by alcohol administration. METHODS: Twelve heavy drinking male participants were scanned on 2 separate days; once after a low dose of alcohol intake (0.4 g/kg), and once after a placebo intake, in balanced order. Images of alcoholic drinks, soft drinks, or neutral objects were shown while participants' neural activity was recorded through fMRI. Moreover, participants' attentional focus was manipulated using a task which required them to process the central images of interest (focus alcohol condition) or a center unattended task (focus not on alcohol condition). RESULTS: Results indicated that an explicit judgment on beverage-related cues increased activation in the prefrontal area compared with the judgment of neutral objects. By comparison with that of task-irrelevant neutral cues, the processing of task-irrelevant alcohol-related cues increased the activation in a large network of cerebral areas including visual and temporal regions, the bilateral anterior cingulate cortex, the posterior cingulate cortex, and the putamen. Moreover, in the condition with focus not on alcohol, the ventral tegmental area (VTA) was particularly activated by the presentation of (task-irrelevant) alcohol-related cues compared to task-irrelevant soft-drink-related cues. CONCLUSIONS: The VTA was especially involved in the automatic processing of alcohol-related cues in young heavy drinkers. Low dose of alcohol did not modulate the neural substrates involved in the processing of salient alcohol-related cues.

Face perception is tuned to horizontal orientation in the N170 time window.

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

The resolution of face perception varies systematically across the visual field.

Visual abilities tend to vary predictably across the visual field-for simple low-level stimuli, visibility is better along the horizontal vs. vertical meridian and in the lower vs. upper visual field. In contrast, face perception abilities have been reported to show either distinct or entirely idiosyncratic patterns of variation in peripheral vision, suggesting a dissociation between the spatial properties of low- and higher-level vision. To assess this link more clearly, we extended methods used in low-level vision to develop an acuity test for face perception, measuring the smallest size at which facial gender can be reliably judged in peripheral vision. In 3 experiments, we show the characteristic inversion effect, with better acuity for upright faces than inverted, demonstrating the engagement of high-level face-selective processes in peripheral vision. We also observe a clear advantage for gender acuity on the horizontal vs. vertical meridian and a smaller-but-consistent lower- vs. upper-field advantage. These visual field variations match those of low-level vision, indicating that higher-level face processing abilities either inherit or actively maintain the characteristic patterns of spatial selectivity found in early vision. The commonality of these spatial variations throughout the visual hierarchy means that the location of faces in our visual field systematically influences our perception of them.

Contributions of low- and high-level contextual mechanisms to human face perception.

Contextual modulations at primary stages of visual processing depend on the strength of local input. Contextual modulations at high-level stages of (face) processing show a similar dependence to local input strength. Namely, the discriminability of a facial feature determines the amount of influence of the face context on that feature. How high-level contextual modulations emerge from primary mechanisms is unclear due to the scarcity of empirical research systematically addressing the functional link between the two. We tested (62) young adults' ability to process local input independent of the context using contrast detection and (upright and inverted) morphed facial feature matching tasks. We first investigated contextual modulation magnitudes across tasks to address their shared variance. A second analysis focused on the profile of performance across contextual conditions. In upright eye matching and contrast detection tasks, contextual modulations only correlated at the level of their profile (averaged Fisher-Z transformed r = 1.18, BF10 > 100), but not magnitude (r = .15, BF10 = .61), suggesting the functional independence but similar working principles of the mechanisms involved. Both the profile (averaged Fisher-Z transformed r = .32, BF10 = 9.7) and magnitude (r = .28, BF10 = 4.58) of the contextual modulations correlated between inverted eye matching and contrast detection tasks. Our results suggest that non-face-specialized high-level contextual mechanisms (inverted faces) work in connection to primary contextual mechanisms, but that the engagement of face-specialized mechanisms for upright faces obscures this connection. Such combined study of low- and high-level contextual modulations sheds new light on the functional relationship between different levels of the visual processing hierarchy, and thus on its functional organization.

From coarse to fine? Spatial and temporal dynamics of cortical face processing.

Primary vision segregates information along 2 main dimensions: orientation and spatial frequency (SF). An important question is how this primary visual information is integrated to support high-level representations. It is generally assumed that the information carried by different SF is combined following a coarse-to-fine sequence. We directly addressed this assumption by investigating how the network of face-preferring cortical regions processes distinct SF over time. Face stimuli were flashed during 75, 150, or 300 ms and masked. They were filtered to preserve low SF (LSF), middle SF (MSF), or high SF (HSF). Most face-preferring regions robustly responded to coarse LSF, face information in early stages of visual processing (i.e., until 75 ms of exposure duration). LSF processing decayed as a function of exposure duration (mostly until 150 ms). In contrast, the processing of fine HSF, face information became more robust over time in the bilateral fusiform face regions and in the right occipital face area. The present evidence suggests the coarse-to-fine strategy as a plausible modus operandi in high-level visual cortex.

Natural Contrast Statistics Facilitate Human Face Categorization.

The ability to detect faces in the environment is of utmost ecological importance for human social adaptation. While face categorization is efficient, fast and robust to sensory degradation, it is massively impaired when the facial stimulus does not match the natural contrast statistics of this visual category, i.e., the typically experienced ordered alternation of relatively darker and lighter regions of the face. To clarify this phenomenon, we characterized the contribution of natural contrast statistics to face categorization. Specifically, 31 human adults viewed various natural images of nonface categories at a rate of 12 Hz, with highly variable images of faces occurring every eight stimuli (1.5 Hz). As in previous studies, neural responses at 1.5 Hz as measured with high-density electroencephalography (EEG) provided an objective neural index of face categorization. Here, when face images were shown in their naturally experienced contrast statistics, the 1.5-Hz face categorization response emerged over occipito-temporal electrodes at very low contrast [5.1%, or 0.009 root-mean-square (RMS) contrast], quickly reaching optimal amplitude at 22.6% of contrast (i.e., RMS contrast of 0.041). Despite contrast negation preserving an image's spectral and geometrical properties, negative contrast images required twice as much contrast to trigger a face categorization response, and three times as much to reach optimum. These observations characterize how the internally stored natural contrast statistics of the face category facilitate visual processing for the sake of fast and efficient face categorization.

The horizontal tuning of face perception relies on the processing of intermediate and high spatial frequencies.

It was recently shown that expert face perception relies on the extraction of horizontally oriented visual cues. Picture-plane inversion was found to eliminate horizontal, suggesting that this tuning contributes to the specificity of face processing. The present experiments sought to determine the spatial frequency (SF) scales supporting the horizontal tuning of face perception. Participants were instructed to match upright and inverted faces that were filtered both in the frequency and orientation domains. Faces in a pair contained horizontal or vertical ranges of information in low, middle, or high SF (LSF, MSF, or HSF). Our findings confirm that upright (but not inverted) face perception is tuned to horizontal orientation. Horizontal tuning was the most robust in the MSF range, next in the HSF range, and absent in the LSF range. Moreover, face inversion selectively disrupted the ability to process horizontal information in MSF and HSF ranges. This finding was replicated even when task difficulty was equated across orientation and SF at upright orientation. Our findings suggest that upright face perception is tuned to horizontally oriented face information carried by intermediate and high SF bands. They further indicate that inversion alters the sampling of face information both in the orientation and SF domains.

Characterizing the spatio-temporal dynamics of the neural events occurring prior to and up to overt recognition of famous faces.

Although it is generally acknowledged that familiar face recognition is fast, mandatory, and proceeds outside conscious control, it is still unclear whether processes leading to familiar face recognition occur in a linear (i.e., gradual) or a nonlinear (i.e., all-or-none) manner. To test these two alternative accounts, we recorded scalp ERPs while participants indicated whether they recognize as familiar the faces of famous and unfamiliar persons gradually revealed in a descending sequence of frames, from the noisier to the least noisy. This presentation procedure allowed us to characterize the changes in scalp ERP responses occurring prior to and up to overt recognition. Our main finding is that gradual and all-or-none processes are possibly involved during overt recognition of familiar faces. Although the N170 and the N250 face-sensitive responses displayed an abrupt activity change at the moment of overt recognition of famous faces, later ERPs encompassing the N400 and late positive component exhibited an incremental increase in amplitude as the point of recognition approached. In addition, famous faces that were not overtly recognized at one trial before recognition elicited larger ERP potentials than unfamiliar faces, probably reflecting a covert recognition process. Overall, these findings present evidence that recognition of familiar faces implicates spatio-temporally complex neural processes exhibiting differential pattern activity changes as a function of recognition state.

Contrast versus identity encoding in the face image follow distinct orientation selectivity profiles.

Orientation selectivity is a fundamental property of primary visual encoding. High-level processing stages also show some form of orientation dependence, with face identification preferentially relying on horizontally-oriented information. How high-level orientation tuning emerges from primary orientation biases is unclear. In the same group of participants, we derived the orientation selectivity profile at primary and high-level visual processing stages using a contrast detection and an identity matching task. To capture the orientation selectivity profile, we calculated the difference in performance between all tested orientations (0, 45, 90, and 135°) for each task and for upright and inverted faces, separately. Primary orientation selectivity was characterized by higher sensitivity to oblique as compared to cardinal orientations. The orientation profile of face identification showed superior horizontal sensitivity to face identity. In each task, performance with upright and inverted faces projected onto qualitatively similar a priori models of orientation selectivity. Yet the fact that the orientation selectivity profiles of contrast detection in upright and inverted faces correlated significantly while such correlation was absent for identification indicates a progressive dissociation of orientation selectivity profiles from primary to high-level stages of orientation encoding. Bayesian analyses further indicate a lack of correlation between the orientation selectivity profiles in the contrast detection and face identification tasks, for upright and inverted faces. From these findings, we conclude that orientation selectivity shows distinct profiles at primary and high-level stages of face processing and that a transformation must occur from general cardinal attenuation when processing basic properties of the face image to horizontal tuning when encoding more complex properties such as identity.

Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information?

Rapidly decoding the emotional content of a face is an important skill for successful social behavior. Several Event Related brain Potential (ERP) have indicated that emotional expressions already influence brain activity as early as 100 ms. Some studies hypothesized that this early brain response to fear depends on coarse-magnocellular inputs, which are primarily driven by Low Spatial Frequency (LSF) cues. Until now however, evidence is inconclusive probably due to the divergent methods used to match luminance and contrast across spatial frequencies and emotional stimuli. In the present study, we measured ERPs to LSF and HSF faces with fearful or neutral expressions when contrast and luminance was matched across SF or not. Our findings clearly show that fearful facial expressions increases the amplitude of P1 (only for contrast-luminance equated images) and N170 in comparison to neutral faces but only in LSF faces, irrespective of contrast or luminance equalization, further suggesting that LSF information plays a crucial role in the early brain responses to fear. Furthermore, we found that, irrespective of luminance or contrast equalization, N170 occurred faster when perceiving LSF faces than HSF faces, again emphasizing the primacy of LSF processing in early face perception.

Fixed or flexible? Orientation preference in identity and gaze processing in humans.

Vision begins with the encoding of contrast at specific orientations. Several works showed that humans identify their conspecifics best based on the horizontally-oriented information contained in the face image; this range conveys the main morphological features of the face. In contrast, the vertical structure of the eye region seems to deliver optimal cues to gaze direction. The present work investigates whether the human face processing system flexibly tunes to vertical information contained in the eye region when processing gaze direction. Alternatively, face processing may invariantly rely on the horizontal range, supporting the domain specificity of orientation tuning for faces and the gateway role of horizontal content to access any type of facial information. Participants judged the gaze direction of faces staring at a range of lateral positions. They additionally performed an identification task with upright and inverted face stimuli. Across tasks, stimuli were filtered to selectively reveal horizontal (H), vertical (V), or combined (HV) information. Most participants identified faces better based on horizontal than vertical information confirming the horizontal tuning of face identification. In contrast, they showed a vertically-tuned sensitivity to gaze direction. The logistic functions fitting the "left" and "right" response proportion as a function of gaze direction were indeed steeper when based on vertical than on horizontal information. The finding of a vertically-tuned processing of gaze direction favours the hypothesis that visual encoding of face information flexibly switches to the orientation channel carrying the cues most relevant to the task at hand. It suggests that horizontal structure, though predominant in the face stimulus, is not a mandatory gateway for efficient face processing. The present evidence may help better understand how visual signals travel the visual system to enable rich and complex representations of naturalistic stimuli such as faces.

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.

The horizontal and vertical relations in upright faces are transmitted by different spatial frequency ranges.

Faces convey distinct types of information: features and their spatial relations, which are differentially vulnerable to inversion. While inversion largely disrupts the processing of vertical spatial relations (e.g. eyes' height), its effect is moderate for horizontal relations (e.g. interocular distance) and local feature properties. The SF ranges optimally transmitting horizontal and vertical face relations were here investigated to further address their functional role in face perception. Participants matched upright and inverted pairs of faces that differed at the level of local featural properties, horizontal relations in vertical relations. Irrespective of SF, the inversion effect was larger for vertical than horizontal and featural cues. Most interestingly, SF differentially influenced the processing of vertical, horizontal and featural cues in upright faces. Vertical relations were optimally processed in intermediate SF, which are known to carry useful information for face individuation. In contrast, horizontal relations were best conveyed by high SF, which are involved in the processing of local face properties. These findings not only confirm that horizontal and vertical relations play distinct functional roles in face perception, but they also further suggest a unique role of vertical relations in face individuation.