From single cells to social perception

Research describing the cellular coding of faces in non-human primates often provides the underlying physiological framework for our understanding of face processing in humans. Models of face perception, explanations of perceptual after-effects from viewing particular types of faces, and interpretation of human neuroimaging data rely on monkey neurophysiological data and the assumption that neurophysiological responses of humans are comparable to those recorded in the non-human primate. Here, we review studies that describe cells that preferentially respond to faces, and assess the link between the physiological characteristics of single cells and social perception. Principally, we describe cells recorded from the non-human primate, although a limited number of cells have been recorded in humans, and are included in order to appraise the validity of non-human physiological data for our understanding of human face and social perception.     

Sex-contingent face after-effects suggest distinct neural populations code male and female faces

Exposure to faces biases perceptions of subsequently viewed faces. Faces similar to those seen previously are judged more normal and attractive than they were prior to exposure. Here we show sex-contingent after-effects following adaptation to eye-spacing (experiment 1), facial identity (experiment 2) and masculinity (experiment 3). Viewing faces of one sex with increased eye-spacing and faces of the other sex with decreased eye-spacing simultaneously induced opposite after-effects for male and female faces (assessed by normality judgments). Viewing faces transformed in identity or masculinity increased preferences for novel faces with characteristics similar to those viewed only when the sex of the faces presented in the adaptation phase and in post-adaptation preference tests were congruent. Because after-effects reflect changes in responses of neural populations that code faces, our findings indicate that distinct neural populations code male and female faces.     

高级视皮层可塑性:物体和面孔知觉学习综述

复杂刺激的知觉学习是指由训练或经验引起的对物体或者面孔等复杂视觉刺激在知觉上长期稳定的改变,一般认为这反映了大脑高级视皮层的可塑性.对简单刺激知觉学习特性的研究已经揭示了低级视皮层的部分可塑性,但是复杂刺激知觉学习的神经机制目前仍存在争议.本文介绍了知觉学习的理论模型和实验证据,并重点探讨了复杂刺激如物体和面孔知觉学习的特性、神经机制及研究方法.该领域未来需要在复杂刺激知觉学习的持久性、面孔不同属性知觉学习的机制,以及复杂刺激知觉学习的理论模型方面做进一步研究.     

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.     

The segregation and integration of colour in motion processing revealed by motion after-effects

Analysis of the colour and motion of objects is widely believed to take place within segregated processing pathways in the primate visual system. However, it is apparent that this segregation cannot remain absolute and that there must be some capacity for integration across these sub-modalities. In this study, we have assessed the extent to which colour constitutes a separable entity in human motion processing by measuring the chromatic selectivity of two kinds of after-effect resulting from motion adaptation. First, the traditional motion after-effect, where prolonged inspection of a unidirectional moving stimulus results in illusory motion in the opposite direction, was found to exhibit a high degree of chromatic selectivity. The second type of after-effect, in which motion adaptation induces misperceptions in the spatial position of stationary objects, was completely insensitive to chromatic composition. This dissociation between the chromatic selectivities of these after-effects shows that chromatic inputs remain segregated at early stages of motion analysis, while at higher levels of cortical processing there is integration across chromatic, as well as achromatic inputs, to produce a unified perceptual output.     

Colour spaces in ecology and evolutionary biology

The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best‐known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species‐specific, more complex models giving accurate but context‐dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log–linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.     

Visual discrimination of primate species based on faces in chimpanzees

Many primate studies have investigated discrimination of individual faces within the same species. However, few studies have looked at discrimination between primate species faces at the categorical level. This study systematically examined the factors important for visual discrimination between primate species faces in chimpanzees, including: colour, orientation, familiarity, and perceptual similarity. Five adult female chimpanzees were tested on their ability to discriminate identical and categorical (non-identical) images of different primate species faces in a series of touchscreen matching-to-sample experiments. Discrimination performance for chimpanzee, gorilla, and orangutan faces was better in colour than in greyscale. An inversion effect was also found, with higher accuracy for upright than inverted faces. Discrimination performance for unfamiliar (baboon and capuchin monkey) and highly familiar (chimpanzee and human) but perceptually different species was equally high. After excluding effects of colour and familiarity, difficulty in discriminating between different species faces can be best explained by their perceptual similarity to each other. Categorical discrimination performance for unfamiliar, perceptually similar faces (gorilla and orangutan) was significantly worse than unfamiliar, perceptually different faces (baboon and capuchin monkey). Moreover, multidimensional scaling analysis of the image similarity data based on local feature matching revealed greater similarity between chimpanzee, gorilla and orangutan faces than between human, baboon and capuchin monkey faces. We conclude our chimpanzees appear to perceive similarity in primate faces in a similar way to humans. Information about perceptual similarity is likely prioritized over the potential influence of previous experience or a conceptual representation of species for categorical discrimination between species faces.     

Visual adaptation to masculine and feminine faces influences generalized preferences and perceptions of trustworthiness

Although previous studies of individual differences in preferences for masculinity in male faces have typically emphasized the importance of factors such as changes in levels of sex hormones during the menstrual cycle, other research has demonstrated that recent visual experience with faces also influences preferences for sexual dimorphism in faces. Adaptation to either masculine or feminine faces increases preferences for novel faces that are similar to those that were recently seen. Here, we replicate this effect and demonstrate that adaptation to masculine or feminine faces also influences the extent to which masculine faces are perceived as trustworthy. These adaptation effects may reflect a proximate mechanism that contributes to the development of face preferences within individuals, underpins phenomena such as imprinting-like effects and condition-dependent face preferences, and shapes personality attributions to faces that play an important role in romantic partner and associate choices. Furthermore, our findings also support the proposal that visual exposure alone cannot explain the context specificity of attitudes to self-resemblance in faces.     

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.     

Functional segregation and temporal hierarchy of the visual perceptive systems.

In extending our previous work, we addressed the question of whether different visual attributes are perceived separately when they belong to different objects, rather than the same one. Using our earlier psychophysical method, but separating the attributes to be paired in two different halves of the screen, we found that human subjects misbind the colour and the direction of motion, or the colour and the orientation of lines, because colour, form, and motion are perceived separately and at different times. The results therefore show that there is a perceptual temporal hierarchy in vision.     

Adaptation improves discrimination of face identity

Whether face adaptation confers any advantages to perceptual processing remains an open question. We investigated whether face adaptation can enhance the ability to make fine discriminations in the vicinity of the adapted face. We compared face discrimination thresholds in three adapting conditions: (i) same-face: where adapting and test faces were the same, (ii) different-face: where adapting and test faces differed, and (iii) baseline: where the adapting stimulus was a blank. Discrimination thresholds for morphed identity changes involving the adapted face (same-face) improved compared with those from both the baseline (no-adaptation) and different-face conditions. Since adapting to a face did not alter discrimination performance for other faces, this effect is selective for the facial identity that is adapted. These results indicate a form of gain control to heighten perceptual sensitivity in the vicinity of a currently viewed face, analogous to forms of adaptive gain control at lower levels of the visual system.     

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.     

Evidence against perceptual bias views for symmetry preferences in human faces

Symmetrical human faces are attractive. Two explanations have been proposed to account for symmetry preferences: (i) the evolutionary advantage view, which posits that symmetry advertises mate quality and (ii) the perceptual bias view, which posits that symmetry preferences are a consequence of greater ease of processing symmetrical images in the visual system. Here, we show that symmetry preferences are greater when face images are upright than when inverted. This is evidence against a simple perceptual bias view, which suggests symmetry preference should be constant across orientation about a vertical axis. We also show that symmetry is preferred even in familiar faces, a finding that is unexpected by perceptual bias views positing that symmetry is only attractive because it represents a familiar prototype of that particular class of stimuli.     

Transfer of tilt after-effects between second-order cues

Second-order cues are visual stimuli that are detectable by human observers, without eliciting a peak in Fourier energy that corresponds to their perceptual properties. The most commonly studied exemplars of second-order cues are those defined by modulation of local contrast (CM). It is widely accepted that such cues are initially detected separately from first-order, luminance modulated (LM), cues. However, after-effects have been shown to transfer between first- and second-order cues (LM and CM, respectively). This suggests the existence of a late link in the mechanisms that subserve their processing. To extend the investigation of the mechanisms for processing second-order cues we consider cues defined by modulations in local orientation (OM). Using a tilt-after-effect (TAE) paradigm, we found partial transfer of adaptation between LM and OM cues, confirming the presence of a link between first and second-order cues. Furthermore, we found a partial transfer of TAE between OM and CM cues. These results suggest that, at or before the site of adaptation, information from all visual cues is combined. However, as transfer of adaptation is below 100% in all cases, this is only a partial integration of information.     

Super-Memorizers Are Not Super-Recognizers

Humans have a natural expertise in recognizing faces. However, the nature of the interaction between this critical visual biological skill and memory is yet unclear. Here, we had the unique opportunity to test two individuals who have had exceptional success in the World Memory Championships, including several world records in face-name association memory. We designed a range of face processing tasks to determine whether superior/expert face memory skills are associated with distinctive perceptual strategies for processing faces. Superior memorizers excelled at tasks involving associative face-name learning. Nevertheless, they were as impaired as controls in tasks probing the efficiency of the face system: face inversion and the other-race effect. Super memorizers did not show increased hippocampal volumes, and exhibited optimal generic eye movement strategies when they performed complex multi-item face-name associations. Our data show that the visual computations of the face system are not malleable and are robust to acquired expertise involving extensive training of associative memory.     

Evaluation of a shape-based model of human face discrimination using FMRI and behavioral techniques

Understanding the neural mechanisms underlying object recognition is one of the fundamental challenges of visual neuroscience. While neurophysiology experiments have provided evidence for a "simple-to-complex" processing model based on a hierarchy of increasingly complex image features, behavioral and fMRI studies of face processing have been interpreted as incompatible with this account. We present a neurophysiologically plausible, feature-based model that quantitatively accounts for face discrimination characteristics, including face inversion and "configural" effects. The model predicts that face discrimination is based on a sparse representation of units selective for face shapes, without the need to postulate additional, "face-specific" mechanisms. We derive and test predictions that quantitatively link model FFA face neuron tuning, neural adaptation measured in an fMRI rapid adaptation paradigm, and face discrimination performance. The experimental data are in excellent agreement with the model prediction that discrimination performance should asymptote as faces become dissimilar enough to activate different neuronal populations.     

Pollinating birds differ in spectral sensitivity

Pollinating animals and their angiosperm hosts often show strong co-adaptation in traits that increase the likelihood of a successful transfer of pollen and nutrient rewards. One such adaptation is the reported colour difference caused by unequal distribution of anthocyanidin pigments amongst plant species visited by hummingbirds and passerines. This phenomenon has been suggested to reflect possible differences in the colour vision of these pollinating birds. The presence of any such difference in colour vision would arguably affect the ecological and evolutionary interactions between flowers and their visitors, accentuating differences in floral displays and attractiveness of plants to the favoured avian pollinators. We have tested for differences in colour vision, as indicated by the amino acid present at certain key positions in the short-wavelength-sensitive type 1 (SWS1) visual pigment opsin, between the major groups of pollinating birds: the non-passerine Trochilidae (hummingbirds), the passerine Meliphagidae (honeyeaters) and Nectariniidae (sunbirds) plus five other Passerida passerine families. The results reveal gross spectral sensitivity differences between hummingbirds and honeyeaters, on the one hand, and the Passerida species, on the other.     

Adaptation Aftereffects in Vocal Emotion Perception Elicited by Expressive Faces and Voices

The perception of emotions is often suggested to be multimodal in nature, and bimodal as compared to unimodal (auditory or visual) presentation of emotional stimuli can lead to superior emotion recognition. In previous studies, contrastive aftereffects in emotion perception caused by perceptual adaptation have been shown for faces and for auditory affective vocalization, when adaptors were of the same modality. By contrast, crossmodal aftereffects in the perception of emotional vocalizations have not been demonstrated yet. In three experiments we investigated the influence of emotional voice as well as dynamic facial video adaptors on the perception of emotion-ambiguous voices morphed on an angry-to-happy continuum. Contrastive aftereffects were found for unimodal (voice) adaptation conditions, in that test voices were perceived as happier after adaptation to angry voices, and vice versa. Bimodal (voice + dynamic face) adaptors tended to elicit larger contrastive aftereffects. Importantly, crossmodal (dynamic face) adaptors also elicited substantial aftereffects in male, but not in female participants. Our results (1) support the idea of contrastive processing of emotions (2), show for the first time crossmodal adaptation effects under certain conditions, consistent with the idea that emotion processing is multimodal in nature, and (3) suggest gender differences in the sensory integration of facial and vocal emotional stimuli.     

A Cross‐Cultural Comparison of Population‐Specific Face Shape Preferences (Homo sapiens)

A substantial number of studies indicate that human facial features such as symmetry and averageness are preferred in human mate choice. Little is known, however, about face preferences in intrapopulation or between‐cultural settings as only a few studies have addressed this topic. One hypothesis is that people prefer faces that resemble faces from their own population as a result of visual adaptation. Here, we present results of an internet‐based experiment in which male and female participants from two European nations, Poland and Scotland, were asked to choose between ‘Polish‐modified’ and ‘Scottish‐modified’ faces (i.e. face portraits modified along one of ten different dimensions to resemble faces of the respective populations) of both sexes while being unaware of the origins of the portraits. The results show that the preferences of Polish judges for Polish‐shaped faces were significantly stronger than the preferences of Scottish judges for the Scottish‐shaped faces. Moreover, both Polish and Scottish judges preferred Polish‐shaped faces to Scottish‐shaped faces. These results suggest that natural visual experience acquired in everyday interpersonal interactions may have limited influence on aesthetic preferences in these particular intrapopulation settings.