The dynamics of visual adaptation to faces

Several recent demonstrations using visual adaptation have revealed high-level aftereffects for complex patterns including faces. While traditional aftereffects involve perceptual distortion of simple attributes such as orientation or colour that are processed early in the visual cortical hierarchy, face adaptation affects perceived identity and expression, which are thought to be products of higher-order processing. And, unlike most simple aftereffects, those involving faces are robust to changes in scale, position and orientation between the adapting and test stimuli. These differences raise the question of how closely related face aftereffects are to traditional ones. Little is known about the build-up and decay of the face aftereffect, and the similarity of these dynamic processes to traditional aftereffects might provide insight into this relationship. We examined the effect of varying the duration of both the adapting and test stimuli on the magnitude of perceived distortions in face identity. We found that, just as with traditional aftereffects, the identity aftereffect grew logarithmically stronger as a function of adaptation time and exponentially weaker as a function of test duration. Even the subtle aspects of these dynamics, such as the power-law relationship between the adapting and test durations, closely resembled that of other aftereffects. These results were obtained with two different sets of face stimuli that differed greatly in their low-level properties. We postulate that the mechanisms governing these shared dynamics may be dissociable from the responses of feature-selective neurons in the early visual cortex.     

Facial Expression Aftereffect Revealed by Adaption to Emotion-Invisible Dynamic Bubbled Faces

Visual adaptation is a powerful tool to probe the short-term plasticity of the visual system. Adapting to local features such as the oriented lines can distort our judgment of subsequently presented lines, the tilt aftereffect. The tilt aftereffect is believed to be processed at the low-level of the visual cortex, such as V1. Adaptation to faces, on the other hand, can produce significant aftereffects in high-level traits such as identity, expression, and ethnicity. However, whether face adaptation necessitate awareness of face features is debatable. In the current study, we investigated whether facial expression aftereffects (FEAE) can be generated by partially visible faces. We first generated partially visible faces using the bubbles technique, in which the face was seen through randomly positioned circular apertures, and selected the bubbled faces for which the subjects were unable to identify happy or sad expressions. When the subjects adapted to static displays of these partial faces, no significant FEAE was found. However, when the subjects adapted to a dynamic video display of a series of different partial faces, a significant FEAE was observed. In both conditions, subjects could not identify facial expression in the individual adapting faces. These results suggest that our visual system is able to integrate unrecognizable partial faces over a short period of time and that the integrated percept affects our judgment on subsequently presented faces. We conclude that FEAE can be generated by partial face with little facial expression cues, implying that our cognitive system fills-in the missing parts during adaptation, or the subcortical structures are activated by the bubbled faces without conscious recognition of emotion during adaptation.     

Reduced Face Aftereffects in Autism Are Not Due to Poor Attention

This study aimed to determine why face identity aftereffects are diminished in children with autism, relative to typical children. To address the possibility that reduced face aftereffects might reflect reduced attention to adapting stimuli, we investigated the consequence of controlling attention to adapting faces during a face identity aftereffect task in children with autism and typical children. We also included a size-change between adaptation and test stimuli to determine whether the reduced aftereffects reflect atypical adaptation to low- or higher-level stimulus properties. Results indicated that when attention was controlled and directed towards adapting stimuli, face identity aftereffects in children with autism were significantly reduced relative to typical children. This finding challenges the notion that atypicalities in the quality and/or quantity of children’s attention during adaptation might account for group differences previously observed in this paradigm. Additionally, evidence of diminished face identity aftereffects despite a stimulus size change supports an adaptive processing atypicality in autism that extends beyond low-level, retinotopically coded stimulus properties. These findings support the notion that diminished face aftereffects in autism reflect atypicalities in adaptive norm-based coding, which could also contribute to face processing difficulties in this group.     

Adaptor Identity Modulates Adaptation Effects in Familiar Face Identification and Their Neural Correlates

Adaptation-related aftereffects (AEs) show how face perception can be altered by recent perceptual experiences. Along with contrastive behavioural biases, modulations of the early event-related potentials (ERPs) were typically reported on categorical levels. Nevertheless, the role of the adaptor stimulus per se for face identity-specific AEs is not completely understood and was therefore investigated in the present study. Participants were adapted to faces (S1s) varying systematically on a morphing continuum between pairs of famous identities (identities A and B), or to Fourier phase-randomized faces, and had to match the subsequently presented ambiguous faces (S2s; 50/50% identity A/B) to one of the respective original faces. We found that S1s identical with or near to the original identities led to strong contrastive biases with more identity B responses following A adaptation and vice versa. In addition, the closer S1s were to the 50/50% S2 on the morphing continuum, the smaller the magnitude of the AE was. The relation between S1s and AE was, however, not linear. Additionally, stronger AEs were accompanied by faster reaction times. Analyses of the simultaneously recorded ERPs revealed categorical adaptation effects starting at 100 ms post-stimulus onset, that were most pronounced at around 125–240 ms for occipito-temporal sites over both hemispheres. S1-specific amplitude modulations were found at around 300–400 ms. Response-specific analyses of ERPs showed reduced voltages starting at around 125 ms when the S1 biased perception in a contrastive way as compared to when it did not. Our results suggest that face identity AEs do not only depend on physical differences between S1 and S2, but also on perceptual factors, such as the ambiguity of S1. Furthermore, short-term plasticity of face identity processing might work in parallel to object-category processing, and is reflected in the first 400 ms of the ERP.     

Visual adaptation and face perception

The appearance of faces can be strongly affected by the characteristics of faces viewed previously. These perceptual after-effects reflect processes of sensory adaptation that are found throughout the visual system, but which have been considered only relatively recently in the context of higher level perceptual judgements. In this review, we explore the consequences of adaptation for human face perception, and the implications of adaptation for understanding the neural-coding schemes underlying the visual representation of faces. The properties of face after-effects suggest that they, in part, reflect response changes at high and possibly face-specific levels of visual processing. Yet, the form of the after-effects and the norm-based codes that they point to show many parallels with the adaptations and functional organization that are thought to underlie the encoding of perceptual attributes like colour. The nature and basis for human colour vision have been studied extensively, and we draw on ideas and principles that have been developed to account for norms and normalization in colour vision to consider potential similarities and differences in the representation and adaptation of faces.     

Atypicalities in Perceptual Adaptation in Autism Do Not Extend to Perceptual Causality

A recent study showed that adaptation to causal events (collisions) in adults caused subsequent events to be less likely perceived as causal. In this study, we examined if a similar negative adaptation effect for perceptual causality occurs in children, both typically developing and with autism. Previous studies have reported diminished adaptation for face identity, facial configuration and gaze direction in children with autism. To test whether diminished adaptive coding extends beyond high-level social stimuli (such as faces) and could be a general property of autistic perception, we developed a child-friendly paradigm for adaptation of perceptual causality. We compared the performance of 22 children with autism with 22 typically developing children, individually matched on age and ability (IQ scores). We found significant and equally robust adaptation aftereffects for perceptual causality in both groups. There were also no differences between the two groups in their attention, as revealed by reaction times and accuracy in a change-detection task. These findings suggest that adaptation to perceptual causality in autism is largely similar to typical development and, further, that diminished adaptive coding might not be a general characteristic of autism at low levels of the perceptual hierarchy, constraining existing theories of adaptation in autism.     

Spatial heterogeneity in the perception of face and form attributes

The identity of an object is a fixed property, independent of where it appears, and an effective visual system should capture this invariance [1-3]. However, we now report that the perceived gender of a face is strongly biased toward male or female at different locations in the visual field. The spatial pattern of these biases was distinctive and stable for each individual. Identical neutral faces looked different when they were presented simultaneously at locations maximally biased to opposite genders. A similar effect was observed for perceived age of faces. We measured the magnitude of this perceptual heterogeneity for four other visual judgments: perceived aspect ratio, orientation discrimination, spatial-frequency discrimination, and color discrimination. The effect was sizeable for the aspect ratio task but substantially smaller for the other three tasks. We also evaluated perceptual heterogeneity for facial gender and orientation tasks at different spatial scales. Strong heterogeneity was observed even for the orientation task when tested at small scales. We suggest that perceptual heterogeneity is a general property of visual perception and results from undersampling of the visual signal at spatial scales that are small relative to the size of the receptive fields associated with each visual attribute.     

How Well Do Computer-Generated Faces Tap Face Expertise?

The use of computer-generated (CG) stimuli in face processing research is proliferating due to the ease with which faces can be generated, standardised and manipulated. However there has been surprisingly little research into whether CG faces are processed in the same way as photographs of real faces. The present study assessed how well CG faces tap face identity expertise by investigating whether two indicators of face expertise are reduced for CG faces when compared to face photographs. These indicators were accuracy for identification of own-race faces and the other-race effect (ORE)–the well-established finding that own-race faces are recognised more accurately than other-race faces. In Experiment 1 Caucasian and Asian participants completed a recognition memory task for own- and other-race real and CG faces. Overall accuracy for own-race faces was dramatically reduced for CG compared to real faces and the ORE was significantly and substantially attenuated for CG faces. Experiment 2 investigated perceptual discrimination for own- and other-race real and CG faces with Caucasian and Asian participants. Here again, accuracy for own-race faces was significantly reduced for CG compared to real faces. However the ORE was not affected by format. Together these results signal that CG faces of the type tested here do not fully tap face expertise. Technological advancement may, in the future, produce CG faces that are equivalent to real photographs. Until then caution is advised when interpreting results obtained using CG faces.     

Cross-Category Adaptation: Objects Produce Gender Adaptation in the Perception of Faces

Adaptation aftereffects have been found for low-level visual features such as colour, motion and shape perception, as well as higher-level features such as gender, race and identity in domains such as faces and biological motion. It is not yet clear if adaptation effects in humans extend beyond this set of higher order features. The aim of this study was to investigate whether objects highly associated with one gender, e.g. high heels for females or electric shavers for males can modulate gender perception of a face. In two separate experiments, we adapted subjects to a series of objects highly associated with one gender and subsequently asked participants to judge the gender of an ambiguous face. Results showed that participants are more likely to perceive an ambiguous face as male after being exposed to objects highly associated to females and vice versa. A gender adaptation aftereffect was obtained despite the adaptor and test stimuli being from different global categories (objects and faces respectively). These findings show that our perception of gender from faces is highly affected by our environment and recent experience. This suggests two possible mechanisms: (a) that perception of the gender associated with an object shares at least some brain areas with those responsible for gender perception of faces and (b) adaptation to gender, which is a high-level concept, can modulate brain areas that are involved in facial gender perception through top-down processes.     

Prioritized Detection of Personally Familiar Faces

We investigated whether personally familiar faces are preferentially processed in conditions of reduced attentional resources and in the absence of conscious awareness. In the first experiment, we used Rapid Serial Visual Presentation (RSVP) to test the susceptibility of familiar faces and faces of strangers to the attentional blink. In the second experiment, we used continuous flash interocular suppression to render stimuli invisible and measured face detection time for personally familiar faces as compared to faces of strangers. In both experiments we found an advantage for detection of personally familiar faces as compared to faces of strangers. Our data suggest that the identity of faces is processed with reduced attentional resources and even in the absence of awareness. Our results show that this facilitated processing of familiar faces cannot be attributed to detection of low-level visual features and that a learned unique configuration of facial features can influence preconscious perceptual processing.     

Baboons (Papio papio) spontaneously process the first-order but not second-order configural properties of faces

A two-alternative forced-choice discrimination task was used to assess whether baboons (N=7) spontaneously process qualitative (i.e., first-order) or quantitative (i.e., second-order) variations in the configural arrangement of facial features. Experiment 1 used as test stimuli second-order pictorial faces of humans or baboons in which the mouth and the eyes were rotated upside down relative to the normal face. Baboons readily discriminated two different normal faces but did not discriminate a normal face from its second-order modified version. Experiment 2 used human or baboon faces for which the first-order configural properties had been distorted by reversing the location of the eyes and mouth within the face. Discrimination was prompt with these stimuli. Experiment 3 replicated some of the conditions and the results of experiment 1, thus ruling out possible effects of learning. It is concluded that baboons are more adept at spontaneously processing first- than second-order configural facial properties, similar to what is known in the human developmental literature.     

Is discrimination enhanced at the boundaries of perceptual categories? A negative case

The human visual system imposes discrete perceptual categories on the continuous input space that is represented by the ratios of excitations of the cones in the retina. Is discrimination enhanced at the boundaries between perceptual hues, in the way that discrimination may be enhanced at the boundaries between speech sounds in hearing? In the chromaticity diagram, the locus of unique green separates colours that appear yellowish from those that appear bluish. Using a two-alternative spatial forced choice and an adapting field equivalent to the Daylight Illuminant D65, we measured chromatic discrimination along lines orthogonal to the locus of unique green. In experimental runs interleaved with these performance measurements, we obtained estimates of the phenomenological boundary from the same observers. No enhancement of objectively measured discrimination was observed at the category boundary between yellowish and bluish hues. Instead, thresholds were minimal at chromaticities where the ratio of long-wave to middle-wave cone excitation was the same as that for the background adapting field.     

Contrast adaptation may enhance contrast discrimination

Whether contrast adaptation may enhance contrast discrimination is a question that has remained largely unresolved because of conflicting empirical evidence. Greenlee and Heitger (1988), for example, reported that contrast discrimination may be enhanced after contrast adaptation, while Maattanen and Koenderink (1991) did not. This paper aimed to account for the different conclusions reached by these independent researchers by manipulations of key differences that exist between the two studies. It is shown that contrast discrimination may be enhanced after adaptation, but that these effects can vary markedly across subjects and test conditions. Enhancements in contrast discrimination are reported to be significant when adapting and testing at low levels of contrast, but just significant at higher levels of contrast. For high contrast signals; enhancements are shown to be independent of temporal frequency but dependent upon viewing conditions. Under binocular viewing conditions, enhancements in contrast discrimination thresholds are shown to be significantly higher than under monocular viewing conditions. It is suggested that the different conclusions reached by Greenlee and Heitger and by Maattanen and Koenderink may be explained by their respective differences in viewing conditions. The former study used binocular, while the latter study used monocular viewing with an occluding eyepatch.     

Individuation and holistic processing of faces in rhesus monkeys

Despite considerable evidence that neural activity in monkeys reflects various aspects of face perception, relatively little is known about monkeys' face processing abilities. Two characteristics of face processing observed in humans are a subordinate-level entry point, here, the default recognition of faces at the subordinate, rather than basic, level of categorization, and holistic effects, i.e. perception of facial displays as an integrated whole. The present study used an adaptation paradigm to test whether untrained rhesus macaques (Macaca mulatta) display these hallmarks of face processing. In experiments 1 and 2, macaques showed greater rebound from adaptation to conspecific faces than to other animals at the individual or subordinate level. In experiment 3, exchanging only the bottom half of a monkey face produced greater rebound in aligned than in misaligned composites, indicating that for normal, aligned faces, the new bottom half may have influenced the perception of the whole face. Scan path analysis supported this assertion: during rebound, fixation to the unchanged eye region was renewed, but only for aligned stimuli. These experiments show that macaques naturally display the distinguishing characteristics of face processing seen in humans and provide the first clear demonstration that holistic information guides scan paths for conspecific faces.     

Assessing the potential information content of multicomponent visual signals: a machine learning approach

Careful investigation of the form of animal signals can offer novel insights into their function. Here, we deconstruct the face patterns of a tribe of primates, the guenons (Cercopithecini), and examine the information that is potentially available in the perceptual dimensions of their multicomponent displays. Using standardized colour-calibrated images of guenon faces, we measure variation in appearance both within and between species. Overall face pattern was quantified using the computer vision ‘eigenface’ technique, and eyebrow and nose-spot focal traits were described using computational image segmentation and shape analysis. Discriminant function analyses established whether these perceptual dimensions could be used to reliably classify species identity, individual identity, age and sex, and, if so, identify the dimensions that carry this information. Across the 12 species studied, we found that both overall face pattern and focal trait differences could be used to categorize species and individuals reliably, whereas correct classification of age category and sex was not possible. This pattern makes sense, as guenons often form mixed-species groups in which familiar conspecifics develop complex differentiated social relationships but where the presence of heterospecifics creates hybridization risk. Our approach should be broadly applicable to the investigation of visual signal function across the animal kingdom.     

Viewer-centered object representation in the human visual system revealed by viewpoint aftereffects

Are there neurons representing specific views of objects in the human visual system? A visual selective adaptation method was used to address this question. After visual adaptation to an object viewed either 15 or 30 degrees from one side, when the same object was subsequently presented near the frontal view, the perceived viewing directions were biased in a direction opposite to that of the adapted viewpoint. This aftereffect can be obtained with spatially nonoverlapping adapting and test stimuli, and it depends on the global representation of the adapting stimuli. Viewpoint aftereffects were found within, but not across, categories of objects tested (faces, cars, wire-like objects). The magnitude of this aftereffect depends on the angular difference between the adapting and test viewing angles and grows with increasing duration of adaptation. These results support the existence of object-selective neurons tuned to specific viewing angles in the human visual system.     

Gender in facial representations: a contrast-based study of adaptation within and between the sexes

Face aftereffects are proving to be an effective means of examining the properties of face-specific processes in the human visual system. We examined the role of gender in the neural representation of faces using a contrast-based adaptation method. If faces of different genders share the same representational face space, then adaptation to a face of one gender should affect both same- and different-gender faces. Further, if these aftereffects differ in magnitude, this may indicate distinct gender-related factors in the organization of this face space. To control for a potential confound between physical similarity and gender, we used a Bayesian ideal observer and human discrimination data to construct a stimulus set in which pairs of different-gender faces were equally dissimilar as same-gender pairs. We found that the recognition of both same-gender and different-gender faces was suppressed following a brief exposure of 100 ms. Moreover, recognition was more suppressed for test faces of a different-gender than those of the same-gender as the adaptor, despite the equivalence in physical and psychophysical similarity. Our results suggest that male and female faces likely occupy the same face space, allowing transfer of aftereffects between the genders, but that there are special properties that emerge along gender-defining dimensions of this space.     

Are faces of different species perceived categorically by human observers?

What are the species boundaries of face processing? Using a face-feature morphing algorithm, image series intermediate between human, monkey (macaque), and bovine faces were constructed. Forced-choice judgement of these images showed sharply bounded categories for upright face images of each species. These predicted the perceptual discrimination boundaries for upright monkey-cow and cow-human images, but not human-monkey images. Species categories were also well-judged for inverted face images, but these did not give sharpened discrimination (categorical perception) at the category boundaries. While categorical species judgements are made reliably, only the distinction between primate faces and cow faces appears to be categorically perceived, and only in upright faces. One inference is that humans may judge monkey faces in terms of human characteristics, albeit distinctive ones.     

Ignored Faces Produce Figural Face Aftereffects

Following adaptation to faces with contracted (or expanded) internal features, faces previously perceived as normal appear distorted in the opposite direction. This figural face aftereffect suggests face-coding mechanisms adapt to changes in the spatial relations of features and/or the global structure of faces. Here, we investigated whether the figural aftereffect requires spatial attention. Participants ignored a distorted adapting face and performed a highly demanding letter-count task. Before and after adaptation, participants rated the normality of morphed distorted faces ranging from 50% contracted through undistorted to 50% expanded. A robust aftereffect was observed. These results suggest that the figural face aftereffect can occur in the absence of spatial attention, even when the attentional demands of the relevant task are high.     

Abnormal adaptive face-coding mechanisms in children with autism spectrum disorder

In low-level vision, exquisite sensitivity to variation in luminance is achieved by adaptive mechanisms that adjust neural sensitivity to the prevailing luminance level. In high-level vision, adaptive mechanisms contribute to our remarkable ability to distinguish thousands of similar faces [1]. A clear example of this sort of adaptive coding is the face-identity aftereffect [2, 3, 4, 5], in which adaptation to a particular face biases perception toward the opposite identity. Here we investigated face adaptation in children with autism spectrum disorder (ASD) by asking them to discriminate between two face identities, with and without prior adaptation to opposite-identity faces. The ASD group discriminated the identities with the same precision as did the age- and ability-matched control group, showing that face identification per se was unimpaired. However, children with ASD showed significantly less adaptation than did their typical peers, with the amount of adaptation correlating significantly with current symptomatology, and face aftereffects of children with elevated symptoms only one third those of controls. These results show that although children with ASD can learn a simple discrimination between two identities, adaptive face-coding mechanisms are severely compromised, offering a new explanation for previously reported face-perception difficulties [6, 7, 8] and possibly for some of the core social deficits in ASD [9, 10].