Specialized visual learning of facial signals of quality in the paper wasp,Polistes dominula

Some primates and one species of paper wasp recognize faces using specific processing strategies to extract individual identity information from conspecific faces. Explanations for the evolution of face specialization typically focus on the complexity associated with individual recognition because all currently identified species with face specialization use faces for individual recognition. In the present study, we show an independent evolution of face specialization in a paper wasp species with facial patterns that signal quality rather than individual identity. Quality signals are simpler to process than individual identity signals because quality signals do not require simultaneous integration across multiple stimuli or learning and memory. Therefore, the results of the present study suggest that the complexity of processing may not be the key factor favouring the evolution of specialization. Instead, the predictable location of socially important signals relative to other anatomical features may allow easy categorization of features, thereby favouring specialized visual processing. Given that visual quality signals are found in many taxa, specific‐processing mechanisms for social signals may be widespread. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 992–997.     

Second-order relational manipulations affect both humans and monkeys

Recognition and individuation of conspecifics by their face is essential for primate social cognition. This ability is driven by a mechanism that integrates the appearance of facial features with subtle variations in their configuration (i.e., second-order relational properties) into a holistic representation. So far, there is little evidence of whether our evolutionary ancestors show sensitivity to featural spatial relations and hence holistic processing of faces as shown in humans. Here, we directly compared macaques with humans in their sensitivity to configurally altered faces in upright and inverted orientations using a habituation paradigm and eye tracking technologies. In addition, we tested for differences in processing of conspecific faces (human faces for humans, macaque faces for macaques) and non-conspecific faces, addressing aspects of perceptual expertise. In both species, we found sensitivity to second-order relational properties for conspecific (expert) faces, when presented in upright, not in inverted, orientation. This shows that macaques possess the requirements for holistic processing, and thus show similar face processing to that of humans.     

The Thatcher illusion in humans and monkeys

Primates possess the remarkable ability to differentiate faces of group members and to extract relevant information about the individual directly from the face. Recognition of conspecific faces is achieved by means of holistic processing, i.e. the processing of the face as an unparsed, perceptual whole, rather than as the collection of independent features (part-based processing). The most striking example of holistic processing is the Thatcher illusion. Local changes in facial features are hardly noticeable when the whole face is inverted (rotated 180°), but strikingly grotesque when the face is upright. This effect can be explained by a lack of processing capabilities for locally rotated facial features when the face is turned upside down. Recently, a Thatcher illusion was described in the macaque monkey analogous to that known from human investigations. Using a habituation paradigm combined with eye tracking, we address the critical follow-up questions raised in the aforementioned study to show the Thatcher illusion as a function of the observer''s species (humans and macaques), the stimulus'' species (humans and macaques) and the level of perceptual expertise (novice, expert).     

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.     

Orientation-contingent face aftereffects and implications for face-coding mechanisms

Humans have an impressive ability to discriminate between faces despite their similarity as visual patterns. This expertise relies on configural coding of spatial relations between face features and/or holistic coding of overall facial structure. These expert face-coding mechanisms appear to be engaged most effectively by upright faces, with inverted faces engaging primarily feature-coding mechanisms. We show that opposite figural aftereffects can be induced simultaneously for upright and inverted faces, demonstrating that distinct neural populations code upright and inverted faces. This result also suggests that expert (upright) face-coding mechanisms can be selectively adapted. These aftereffects occur for judgments of face normality and face gender and are robust to changes in face size, ruling out adaptation of low-level, retinotopically organized coding mechanisms. Our results suggest a resolution of a paradox in the face recognition literature. Neuroimaging studies have found surprisingly little orientation selectivity in the fusiform face area (FFA) despite evidence that this region plays a role in expert face coding and that expert face-coding mechanisms are selectively engaged by upright faces. Our results, demonstrating orientation-contingent adaptation of face-coding mechanisms, suggest that the FFA's apparent lack of orientation selectivity may be an artifact of averaging across distinct populations within the FFA that respond to upright and inverted faces.     

Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way

Most recognition is based on identifying features, but specialization for face recognition in primates relies on a different mechanism, termed ‘holistic processing’ where facial features are bound together into a gestalt which is more than the sum of its parts. Here, we test whether individual face recognition in paper wasps also involved holistic processing using a modification of the classic part-whole test in two related paper wasp species: Polistes fuscatus, which use facial patterns to individually identify conspecifics, and Polistes dominula, which lacks individual recognition. We show that P. fuscatus use holistic processing to discriminate between P. fuscatus face images but not P. dominula face images. By contrast, P. dominula do not rely on holistic processing to discriminate between conspecific or heterospecific face images. Therefore, P. fuscatus wasps have evolved holistic face processing, but this ability is highly specific and shaped by species-specific and stimulus-specific selective pressures. Convergence towards holistic face processing in distant taxa (primates, wasps) as well as divergence among closely related taxa with different recognition behaviour (P. dominula, P. fuscatus) suggests that holistic processing may be a universal adaptive strategy to facilitate expertise in face recognition.     

The Perception of Dynamic and Static Facial Expressions of Happiness and Disgust Investigated by ERPs and fMRI Constrained Source Analysis

A recent functional magnetic resonance imaging (fMRI) study by our group demonstrated that dynamic emotional faces are more accurately recognized and evoked more widespread patterns of hemodynamic brain responses than static emotional faces. Based on this experimental design, the present study aimed at investigating the spatio-temporal processing of static and dynamic emotional facial expressions in 19 healthy women by means of multi-channel electroencephalography (EEG), event-related potentials (ERP) and fMRI-constrained regional source analyses. ERP analysis showed an increased amplitude of the LPP (late posterior positivity) over centro-parietal regions for static facial expressions of disgust compared to neutral faces. In addition, the LPP was more widespread and temporally prolonged for dynamic compared to static faces of disgust and happiness. fMRI constrained source analysis on static emotional face stimuli indicated the spatio-temporal modulation of predominantly posterior regional brain activation related to the visual processing stream for both emotional valences when compared to the neutral condition in the fusiform gyrus. The spatio-temporal processing of dynamic stimuli yielded enhanced source activity for emotional compared to neutral conditions in temporal (e.g., fusiform gyrus), and frontal regions (e.g., ventromedial prefrontal cortex, medial and inferior frontal cortex) in early and again in later time windows. The present data support the view that dynamic facial displays trigger more information reflected in complex neural networks, in particular because of their changing features potentially triggering sustained activation related to a continuing evaluation of those faces. A combined fMRI and EEG approach thus provides an advanced insight to the spatio-temporal characteristics of emotional face processing, by also revealing additional neural generators, not identifiable by the only use of an fMRI approach.     

Face recognition.

The study of face-selective neurons in the monkey temporal lobe, and face recognition deficits in humans after brain damage have both become very active fields of investigation. Face-selective neurons appear to be members of ensembles for coding faces rather than individual face detectors or grandmother cells. They reflect the more general role of temporal cortex in pattern recognition. In humans there are a variety of face-processing impairments that result from damage to different areas, and which reflect interference at different levels of processing of the facial image.     

Neurobiological basis of human recognition of facial emotion

In the review of modern data and ideas concerning the neurophysiological mechanisms and morphological foundations of the most essential communicative function of humans and monkeys, that of recognition of faces and their emotional expressions, the attention is focussed on its dynamic realization and structural provision. On the basis of literature data about hemodynamic and metabolic mapping of the brain the author analyses the role of different zones of the ventral and dorsal visual cortical pathway, the frontal neocortex and amigdala in the facial features processing, as well as the specificity of this processing at each level. Special attention is given to the module principle of the facial processing in the temporal cortex. The dynamic characteristics of facial recognition are discussed according to the electrical evoked response data in healthy and disease humans and monkeys. Modern evidences on the role of different brain structures in the generation of successive evoked response waves in connection with successive stages of facial processing are analyzed. The similarity and differences between mechanisms of recognition of faces and their emotional expression are also considered.     

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.     

Representation of Faces in Longtailed Macaques (Macaca fascicularis)

The experiments described in this study were intended to increase our knowledge about social cognition in primates. Longtailed macaques (Macaca fascicularis) had to discriminate facial drawings of different emotional expressions. A new experimental approach was used. During the experimental sessions social interactions within the group were permitted, but the learning behaviour of individual monkeys was analysed. The procedure consisted of a simultaneous discrimination between four visual patterns under continuous reinforcement. It has implications not only for simple tasks of stimulus discrimination but also for complex problems of internal representations and visual communication. The monkeys learned quickly to discriminate faces of different emotional expressions. This discrimination ability was completely invariant with variations of colour, brightness, size, and rotation. Rotated and inverted faces were recognized perfectly. A preference test for particular features resulted in a graded estimation of particular facial components. Most important for face recognition was the outline, followed by the eye region and the mouth. An asymmetry in recognition of the left and right halves of the face was found. Further tests involving jumbled faces indicated that not only the presence of distinct facial cues but the specific relation of facial features is essential in recognizing faces. The experiment generally confirms that causal mechanisms of social cognition in non-human primates can be studied experimentally. The behavioural results are highly consistent with findings from neurophysiology and research with human subjects.     

Neural Tuning Size in a Model of Primate Visual Processing Accounts for Three Key Markers of Holistic Face Processing

Faces are an important and unique class of visual stimuli, and have been of interest to neuroscientists for many years. Faces are known to elicit certain characteristic behavioral markers, collectively labeled “holistic processing”, while non-face objects are not processed holistically. However, little is known about the underlying neural mechanisms. The main aim of this computational simulation work is to investigate the neural mechanisms that make face processing holistic. Using a model of primate visual processing, we show that a single key factor, “neural tuning size”, is able to account for three important markers of holistic face processing: the Composite Face Effect (CFE), Face Inversion Effect (FIE) and Whole-Part Effect (WPE). Our proof-of-principle specifies the precise neurophysiological property that corresponds to the poorly-understood notion of holism, and shows that this one neural property controls three classic behavioral markers of holism. Our work is consistent with neurophysiological evidence, and makes further testable predictions. Overall, we provide a parsimonious account of holistic face processing, connecting computation, behavior and neurophysiology.     

Non-invasive evaluation of face and motion perception in humans

The neural mechanisms for the perception of face and motion were studied using psychophysical threshold measurements, event-related potentials (ERPs), and functional magnetic resonance imaging (fMRI). A face-specific ERP component, N170, was recorded over the posterior temporal cortex. Removal of the high-spatial-frequency components of the face altered the perception of familiar faces significantly, and familiarity can facilitate the cortico-cortical processing of facial perceptions. Similarly, the high-spatial-frequency components of the face seemed to be crucial for the recognition of facial expressions. Aging and visuospatial impairments affected motion perception significantly. Two distinct components of motion ERPs, N170 and P200, were recorded over the parietal region. The former was related to horizontal motion perception while the latter reflected the perception of radial optic flow motion. The results of fMRI showed that horizontal movements of objects and radial optic flow motion were perceived differently in the V5/MT and superior parietal lobe. We conclude that an integrated approach can provide useful information on spatial and temporal processing of face and motion non-invasively.     

Seeing Life through Positive-Tinted Glasses: Color–Meaning Associations

There is a growing body of literature to show that color can convey information, owing to its emotionally meaningful associations. Most research so far has focused on negative hue–meaning associations (e.g., red) with the exception of the positive aspects associated with green. We therefore set out to investigate the positive associations of two colors (i.e., green and pink), using an emotional facial expression recognition task in which colors provided the emotional contextual information for the face processing. In two experiments, green and pink backgrounds enhanced happy face recognition and impaired sad face recognition, compared with a control color (gray). Our findings therefore suggest that because green and pink both convey positive information, they facilitate the processing of emotionally congruent facial expressions (i.e., faces expressing happiness) and interfere with that of incongruent facial expressions (i.e., faces expressing sadness). Data also revealed a positive association for white. Results are discussed within the theoretical framework of emotional cue processing and color meaning.     

Single-unit responses selective for whole faces in the human amygdala

The human amygdala is critical for social cognition from faces, as borne out by impairments in recognizing facial emotion following amygdala lesions [1] and differential activation of the amygdala by faces [2-5]. Single-unit recordings in the primate amygdala have documented responses selective for faces, their identity, or emotional expression [6, 7], yet how the amygdala represents face information remains unknown. Does it encode specific features of faces that are particularly critical for recognizing emotions (such as the eyes), or does it encode the whole face, a level of representation that might be the proximal substrate for subsequent social cognition? We investigated this question by recording from over 200 single neurons in the amygdalae of seven neurosurgical patients with implanted depth electrodes [8]. We found that approximately half of all neurons responded to faces or parts of faces. Approximately 20% of all neurons responded selectively only to the whole face. Although responding most to whole faces, these neurons paradoxically responded more when only a small part of the face was shown compared to when almost the entire face was shown. We suggest that the human amygdala plays a predominant role in representing global information about faces, possibly achieved through inhibition between individual facial features.     

A stable biologically motivated learning mechanism for visual feature extraction to handle facial categorization

The brain mechanism of extracting visual features for recognizing various objects has consistently been a controversial issue in computational models of object recognition. To extract visual features, we introduce a new, biologically motivated model for facial categorization, which is an extension of the Hubel and Wiesel simple-to-complex cell hierarchy. To address the synaptic stability versus plasticity dilemma, we apply the Adaptive Resonance Theory (ART) for extracting informative intermediate level visual features during the learning process, which also makes this model stable against the destruction of previously learned information while learning new information. Such a mechanism has been suggested to be embedded within known laminar microcircuits of the cerebral cortex. To reveal the strength of the proposed visual feature learning mechanism, we show that when we use this mechanism in the training process of a well-known biologically motivated object recognition model (the HMAX model), it performs better than the HMAX model in face/non-face classification tasks. Furthermore, we demonstrate that our proposed mechanism is capable of following similar trends in performance as humans in a psychophysical experiment using a face versus non-face rapid categorization task.     

Familiar Face Detection in 180ms

The visual system is tuned for rapid detection of faces, with the fastest choice saccade to a face at 100ms. Familiar faces have a more robust representation than do unfamiliar faces, and are detected faster in the absence of awareness and with reduced attentional resources. Faces of family and close friends become familiar over a protracted period involving learning the unique visual appearance, including a view-invariant representation, as well as person knowledge. We investigated the effect of personal familiarity on the earliest stages of face processing by using a saccadic-choice task to measure how fast familiar face detection can happen. Subjects made correct and reliable saccades to familiar faces when unfamiliar faces were distractors at 180ms—very rapid saccades that are 30 to 70ms earlier than the earliest evoked potential modulated by familiarity. By contrast, accuracy of saccades to unfamiliar faces with familiar faces as distractors did not exceed chance. Saccades to faces with object distractors were even faster (110 to 120 ms) and equivalent for familiar and unfamiliar faces, indicating that familiarity does not affect ultra-rapid saccades. We propose that detectors of diagnostic facial features for familiar faces develop in visual cortices through learning and allow rapid detection that precedes explicit recognition of identity.     

Modulation of Alpha Oscillations in the Human EEG with Facial Preference

Facial preference that results from the processing of facial information plays an important role in social interactions as well as the selection of a mate, friend, candidate, or favorite actor. However, it still remains elusive which brain regions are implicated in the neural mechanisms underlying facial preference, and how neural activities in these regions are modulated during the formation of facial preference. In the present study, we investigated the modulation of electroencephalography (EEG) oscillatory power with facial preference. For the reliable assessments of facial preference, we designed a series of passive viewing and active choice tasks. In the former task, twenty-four face stimuli were passively viewed by participants for multiple times in random order. In the latter task, the same stimuli were then evaluated by participants for their facial preference judgments. In both tasks, significant differences between the preferred and non-preferred faces groups were found in alpha band power (8–13 Hz) but not in other frequency bands. The preferred faces generated more decreases in alpha power. During the passive viewing task, significant differences in alpha power between the preferred and non-preferred face groups were observed at the left frontal regions in the early (0.15–0.4 s) period during the 1-s presentation. By contrast, during the active choice task when participants consecutively watched the first and second face for 1 s and then selected the preferred one, an alpha power difference was found for the late (0.65–0.8 s) period over the whole brain during the first face presentation and over the posterior regions during the second face presentation. These results demonstrate that the modulation of alpha activity by facial preference is a top-down process, which requires additional cognitive resources to facilitate information processing of the preferred faces that capture more visual attention than the non-preferred faces.     

Visual search for orientation of faces by a chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>): face-specific upright superiority and the role of facial configural properties

A previous experiment showed that a chimpanzee performed better in searching for a target human face that differed in orientation from distractors when the target had an upright orientation than when targets had inverted or horizontal orientation [Tomonaga (1999a) Primate Res 15:215–229]. This upright superiority effect was also seen when using chimpanzee faces as targets but not when using photographs of a house. The present study sought to extend these results and explore factors affecting the face-specific upright superiority effect. Upright superiority was shown in a visual search for orientation when caricaturized human faces and dog faces were used as stimuli for the chimpanzee but not when shapes of a hand and chairs were presented. Thus, the configural properties of facial features, which cause an inversion effect in face recognition in humans and chimpanzees, were thought to be a source of the upright superiority effect in the visual search process. To examine this possibility, various stimuli manipulations were introduced in subsequent experiments. The results clearly show that the configuration of facial features plays a critical role in the upright superiority effect, and strongly suggest similarity in face processing in humans and chimpanzees.