How dogs scan familiar and inverted faces: an eye movement study

Faces play an important role in communication and identity recognition in social animals. Domestic dogs often respond to human facial cues, but their face processing is weakly understood. In this study, facial inversion effect (deficits in face processing when the image is turned upside down) and responses to personal familiarity were tested using eye movement tracking. A total of 23 pet dogs and eight kennel dogs were compared to establish the effects of life experiences on their scanning behavior. All dogs preferred conspecific faces and showed great interest in the eye area, suggesting that they perceived images representing faces. Dogs fixated at the upright faces as long as the inverted faces, but the eye area of upright faces gathered longer total duration and greater relative fixation duration than the eye area of inverted stimuli, regardless of the species (dog or human) shown in the image. Personally, familiar faces and eyes attracted more fixations than the strange ones, suggesting that dogs are likely to recognize conspecific and human faces in photographs. The results imply that face scanning in dogs is guided not only by the physical properties of images, but also by semantic factors. In conclusion, in a free-viewing task, dogs seem to target their fixations at naturally salient and familiar items. Facial images were generally more attractive for pet dogs than kennel dogs, but living environment did not affect conspecific preference or inversion and familiarity responses, suggesting that the basic mechanisms of face processing in dogs could be hardwired or might develop under limited exposure.     

How do rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) scan faces in a visual paired comparison task?

When novel and familiar faces are viewed simultaneously, humans and monkeys show a preference for looking at the novel face. The facial features attended to in familiar and novel faces, were determined by analyzing the visual exploration patterns, or scanpaths, of four monkeys performing a visual paired comparison task. In this task, the viewer was first familiarized with an image and then it was presented simultaneously with a novel and the familiar image. A looking preference for the novel image indicated that the viewer recognized the familiar image and hence differentiates between the familiar and the novel images. Scanpaths and relative looking preference were compared for four types of images: (1) familiar and novel objects, (2) familiar and novel monkey faces with neutral expressions, (3) familiar and novel inverted monkey faces, and (4) faces from the same monkey with different facial expressions. Looking time was significantly longer for the novel face, whether it was neutral, expressing an emotion, or inverted. Monkeys did not show a preference, or an aversion, for looking at aggressive or affiliative facial expressions. The analysis of scanpaths indicated that the eyes were the most explored facial feature in all faces. When faces expressed emotions such as a fear grimace, then monkeys scanned features of the face, which contributed to the uniqueness of the expression. Inverted facial images were scanned similarly to upright images. Precise measurement of eye movements during the visual paired comparison task, allowed a novel and more quantitative assessment of the perceptual processes involved the spontaneous visual exploration of faces and facial expressions. These studies indicate that non-human primates carry out the visual analysis of complex images such as faces in a characteristic and quantifiable manner.     

Discrimination of familiar human faces in dogs (Canis familiaris)

Faces are an important visual category for many taxa, and the human face is no exception to this. Because faces differ in subtle ways and possess many idiosyncratic features, they provide a rich source of perceptual cues. A fair amount of those cues are learned through social interactions and are used for future identification of individual humans. These effects of individual experience can be studied particularly well in hetero-specific face perception. Domestic dogs represent a perfect model in this respect, due to their proved ability to extract important information from the human face in socio-communicative interactions. There is also suggestive evidence that dogs can identify their owner or other familiar human individuals by using visual information from the face. However, most studies have used only dogs’ looking behavior to examine their visual processing of human faces and it has been demonstrated only that dogs can differentiate between familiar and unknown human faces. Here, we examined the dog's ability to discriminate the faces of two familiar persons by active choice (approach and touch). Furthermore, in successive stages of the experiment we investigated how well dogs discriminate humans in different representations by systematically reducing the informational richness and the quality of the stimuli. We found a huge inter-individual and inter-stage variance in performance, indicating differences across dogs in their learning ability as well as their selection of discriminative cues. On a group level, the performance of dogs significantly decreased when they were presented with pictures of human heads after having learned to discriminate the real heads, and when – after relearning – confronted with the same pictures showing only the inner parts of the heads. However, as two dogs quickly mastered all stages, we conclude that dogs are in principle able to discriminate people on the basis of visual information from their faces and by making active choices.     

Dogs do look at images: eye tracking in canine cognition research

Despite intense research on the visual communication of domestic dogs, their cognitive capacities have not yet been explored by eye tracking. The aim of the current study was to expand knowledge on the visual cognition of dogs using contact-free eye movement tracking under conditions where social cueing and associative learning were ruled out. We examined whether dogs spontaneously look at actual objects within pictures and can differentiate between pictures according to their novelty or categorical information content. Eye movements of six domestic dogs were tracked during presentation of digital color images of human faces, dog faces, toys, and alphabetic characters. We found that dogs focused their attention on the informative regions of the images without any task-specific pre-training and their gazing behavior depended on the image category. Dogs preferred the facial images of conspecifics over other categories and fixated on a familiar image longer than on novel stimuli regardless of the category. Dogs’ attraction to conspecifics over human faces and inanimate objects might reflect their natural interest, but further studies are needed to establish whether dogs possess picture object recognition. Contact-free eye movement tracking is a promising method for the broader exploration of processes underlying special socio-cognitive skills in dogs previously found in behavioral studies.     

Dogs can discriminate human smiling faces from blank expressions

Dogs have a unique ability to understand visual cues from humans. We investigated whether dogs can discriminate between human facial expressions. Photographs of human faces were used to test nine pet dogs in two-choice discrimination tasks. The training phases involved each dog learning to discriminate between a set of photographs of their owner’s smiling and blank face. Of the nine dogs, five fulfilled these criteria and were selected for test sessions. In the test phase, 10 sets of photographs of the owner’s smiling and blank face, which had previously not been seen by the dog, were presented. The dogs selected the owner’s smiling face significantly more often than expected by chance. In subsequent tests, 10 sets of smiling and blank face photographs of 20 persons unfamiliar to the dogs were presented (10 males and 10 females). There was no statistical difference between the accuracy in the case of the owners and that in the case of unfamiliar persons with the same gender as the owner. However, the accuracy was significantly lower in the case of unfamiliar persons of the opposite gender to that of the owner, than with the owners themselves. These results suggest that dogs can learn to discriminate human smiling faces from blank faces by looking at photographs. Although it remains unclear whether dogs have human-like systems for visual processing of human facial expressions, the ability to learn to discriminate human facial expressions may have helped dogs adapt to human society.     

Face processing in humans and new world monkeys: the influence of experiential and ecological factors

This study tests whether the face-processing system of humans and a nonhuman primate species share characteristics that would allow for early and quick processing of socially salient stimuli: a sensitivity toward conspecific faces, a sensitivity toward highly practiced face stimuli, and an ability to generalize changes in the face that do not suggest a new identity, such as a face differently oriented. The look rates by adult tamarins and humans toward conspecific and other primate faces were examined to determine if these characteristics are shared. A visual paired comparison (VPC) task presented subjects with either a human face, chimpanzee face, tamarin face, or an object as a sample, and then a pair containing the previous stimulus and a novel stimulus was presented. The stimuli were either presented all in an upright orientation, or all in an inverted orientation. The novel stimulus in the pair was either an orientation change of the same face/object or a new example of the same type of face/object, and the stimuli were shown either in an upright orientation or in an inverted orientation. Preference to novelty scores revealed that humans attended most to novel individual human faces, and this effect decreased significantly if the stimuli were inverted. Tamarins showed preferential looking toward novel orientations of previously seen tamarin faces in the upright orientation, but not in an inverted orientation. Similarly, their preference to look longer at novel tamarin and human faces within the pair was reduced significantly with inverted stimuli. The results confirmed prior findings in humans that novel human faces generate more attention in the upright than in the inverted orientation. The monkeys also attended more to faces of conspecifics, but showed an inversion effect to orientation change in tamarin faces and to identity changes in tamarin and human faces. The results indicate configural processing restricted to particular kinds of primate faces by a New World monkey species, with configural processing influenced by life experience (human faces and tamarin faces) and specialized to process orientation changes specific to conspecific faces.     

Left gaze bias in humans, rhesus monkeys and domestic dogs

While viewing faces, human adults often demonstrate a natural gaze bias towards the left visual field, that is, the right side of the viewee’s face is often inspected first and for longer periods. Using a preferential looking paradigm, we demonstrate that this bias is neither uniquely human nor limited to primates, and provide evidence to help elucidate its biological function within a broader social cognitive framework. We observed that 6-month-old infants showed a wider tendency for left gaze preference towards objects and faces of different species and orientation, while in adults the bias appears only towards upright human faces. Rhesus monkeys showed a left gaze bias towards upright human and monkey faces, but not towards inverted faces. Domestic dogs, however, only demonstrated a left gaze bias towards human faces, but not towards monkey or dog faces, nor to inanimate object images. Our findings suggest that face- and species-sensitive gaze asymmetry is more widespread in the animal kingdom than previously recognised, is not constrained by attentional or scanning bias, and could be shaped by experience to develop adaptive behavioural significance.     

How do children view and categorise human and dog facial expressions?

Children are often surrounded by other humans and companion animals (e.g., dogs, cats); and understanding facial expressions in all these social partners may be critical to successful social interactions. In an eye-tracking study, we examined how children (4–10 years old) view and label facial expressions in adult humans and dogs. We found that children looked more at dogs than humans, and more at negative than positive or neutral human expressions. Their viewing patterns (Proportion of Viewing Time, PVT) at individual facial regions were also modified by the viewed species and emotion, with the eyes not always being most viewed: this related to positive anticipation when viewing humans, whilst when viewing dogs, the mouth was viewed more or equally compared to the eyes for all emotions. We further found that children's labelling (Emotion Categorisation Accuracy, ECA) was better for the perceived valence than for emotion category, with positive human expressions easier than both positive and negative dog expressions. They performed poorly when asked to freely label facial expressions, but performed better for human than dog expressions. Finally, we found some effects of age, sex, and other factors (e.g., experience with dogs) on both PVT and ECA. Our study shows that children have a different gaze pattern and identification accuracy compared to adults, for viewing faces of human adults and dogs. We suggest that for recognising human (own-face-type) expressions, familiarity obtained through casual social interactions may be sufficient; but for recognising dog (other-face-type) expressions, explicit training may be required to develop competence.

Highlights

• We conducted an eye-tracking experiment to investigate how children view and categorise facial expressions in adult humans and dogs
• Children's viewing patterns were significantly dependent upon the facial region, species, and emotion viewed
• Children's categorisation also varied with the species and emotion viewed, with better performance for valence than emotion categories
• Own-face-types (adult humans) are easier than other-face-types (dogs) for children, and casual familiarity (e.g., through family dogs) to the latter is not enough to achieve perceptual competence

     

Multiple perceptual strategies used by macaque monkeys for face recognition

Successful integration of individuals in macaque societies suggests that monkeys use fast and efficient perceptual mechanisms to discriminate between conspecifics. Humans and great apes use primarily holistic and configural, but also feature-based, processing for face recognition. The relative contribution of these processes to face recognition in monkeys is not known. We measured face recognition in three monkeys performing a visual paired comparison task. Monkey and humans faces were (1) axially rotated, (2) inverted, (3) high-pass filtered, and (4) low-pass filtered to isolate different face processing strategies. The amount of time spent looking at the eyes, mouth, and other facial features was compared across monkey and human faces for each type of stimulus manipulation. For all monkeys, face recognition, expressed as novelty preference, was intact for monkey faces that were axially rotated or spatially filtered and was supported in general by preferential looking at the eyes, but was impaired for inverted faces in two of the three monkeys. Axially rotated, upright human faces with a full range of spatial frequencies were also recognized, however, the distribution of time spent exploring each facial feature was significantly different compared to monkey faces. No novelty preference, and hence no inferred recognition, was observed for inverted or low-pass filtered human faces. High-pass filtered human faces were recognized, however, the looking pattern on facial features deviated from the pattern observed for monkey faces. Taken together these results indicate large differences in recognition success and in perceptual strategies used by monkeys to recognize humans versus conspecifics. Monkeys use both second-order configural and feature-based processing to recognize the faces of conspecifics, but they use primarily feature-based strategies to recognize human faces.     

Are readers of our face readers of our minds? Dogs (<Emphasis Type="Italic">Canis familiaris</Emphasis>) show situation-dependent recognition of human’s attention

The ability of animals to use behavioral/facial cues in detection of human attention has been widely investigated. In this test series we studied the ability of dogs to recognize human attention in different experimental situations (ball-fetching game, fetching objects on command, begging from humans). The attentional state of the humans was varied along two variables: (1) facing versus not facing the dog; (2) visible versus non-visible eyes. In the first set of experiments (fetching) the owners were told to take up different body positions (facing or not facing the dog) and to either cover or not cover their eyes with a blindfold. In the second set of experiments (begging) dogs had to choose between two eating humans based on either the visibility of the eyes or direction of the face. Our results show that the efficiency of dogs to discriminate between attentive and inattentive humans depended on the context of the test, but they could rely on the orientation of the body, the orientation of the head and the visibility of the eyes. With the exception of the fetching-game situation, they brought the object to the front of the human (even if he/she turned his/her back towards the dog), and preferentially begged from the facing (or seeing) human. There were also indications that dogs were sensitive to the visibility of the eyes because they showed increased hesitative behavior when approaching a blindfolded owner, and they also preferred to beg from the person with visible eyes. We conclude that dogs are able to rely on the same set of human facial cues for detection of attention, which form the behavioral basis of understanding attention in humans. Showing the ability of recognizing human attention across different situations dogs proved to be more flexible than chimpanzees investigated in similar circumstances.     

Seeing two faces together: preference formation in humans and rhesus macaques

Humans, great apes and old world monkeys show selective attention to faces depending on conspecificity, familiarity, and social status supporting the view that primates share similar face processing mechanisms. Although many studies have been done on face scanning strategy in monkeys and humans, the mechanisms influencing viewing preference have received little attention. To determine how face categories influence viewing preference in humans and rhesus macaques (Macaca mulatta), we performed two eye-tracking experiments using a visual preference task whereby pairs of faces from different species were presented simultaneously. The results indicated that viewing time was significantly influenced by the pairing of the face categories. Humans showed a strong bias towards an own-race face in an Asian–Caucasian condition. Rhesus macaques directed more attention towards non-human primate faces when they were paired with human faces, regardless of the species. When rhesus faces were paired with faces from Barbary macaques (Macaca sylvanus) or chimpanzees (Pan troglodytes), the novel species’ faces attracted more attention. These results indicate that monkeys’ viewing preferences, as assessed by a visual preference task, are modulated by several factors, species and dominance being the most influential.     

熟悉面孔与陌生面孔识别的差异

摘 要：面孔识别包括熟悉面孔识别和陌生面孔识别,两者之间的差异已经得到了多方面的证明。神经生理学的研究发现,识别陌生面孔和熟悉面孔所激活的脑区存在差异,与识别陌生面孔相比,识别熟悉面孔的脑区活动范围更大,包括双侧前额叶、单侧颞叶、海马回、杏仁核、后扣带回和右下额叶。并且也存在脑电的差异,比如 N400和P600的差异。对陌生面孔和熟悉面孔识别具有相同影响的因素有：遮挡、倒置等;具有不同影响的因素有：视角、表情、内外部特征等。文章也探讨了陌生面孔变成熟悉面孔的过程,以及在这一过程中起主要作用的编码形式等。     

Increased visual interest and affective responses to impossible figures in early infancy

This research evaluated infants’ facial expressions as they viewed pictures of possible and impossible objects on a TV screen. Previous studies in our lab demonstrated that four-month-old infants looked longer at the impossible figures and fixated to a greater extent within the problematic region of the impossible shape, suggesting they were sensitive to novel or unusual object geometry. Our work takes studies of looking time data a step further, determining if increased looking co-occurs with facial expressions associated with increased visual interest and curiosity, or even puzzlement and surprise. We predicted that infants would display more facial expressions consistent with either “interest” or “surprise” when viewing the impossible objects relative to possible ones, which would provide further evidence of increased perceptual processing due to incompatible spatial information. Our results showed that the impossible cubes evoked both longer looking times and more reactive expressions in the majority of infants. Specifically, the data revealed significantly greater frequency of raised eyebrows, widened eyes and returns to looking when viewing impossible figures with the most robust effects occurring after a period of habituation. The pattern of facial expressions were consistent with the “interest” family of facial expressions and appears to reflect infants’ ability to perceive systematic differences between matched pairs of possible and impossible objects as well as recognize novel geometry found in impossible objects. Therefore, as young infants are beginning to register perceptual discrepancies in visual displays, their facial expressions may reflect heightened attention and increased information processing associated with identifying irreconcilable contours in line drawings of objects. This work further clarifies the ongoing formation and development of early mental representations of coherent 3D objects.     

Changes in infant visual attention when observing repeated actions

Infants’ early visual preferences for faces, and their observational learning abilities, are well-established in the literature. The current study examines how infants’ attention changes as they become increasingly familiar with a person and the actions that person is demonstrating. The looking patterns of 12- (n = 61) and 16-month-old infants (n = 29) were tracked while they watched videos of an adult presenting novel actions with four different objects three times. A face-to-action ratio in visual attention was calculated for each repetition and summarized as a mean across all videos. The face-to-action ratio increased with each action repetition, indicating that there was an increase in attention to the face relative to the action each additional time the action was demonstrated. Infant’s prior familiarity with the object used was related to face-to-action ratio in 12-month-olds and initial looking behavior was related to face-to-action ratio in the whole sample. Prior familiarity with the presenter, and infant gender and age, were not related to face-to-action ratio. This study has theoretical implications for face preference and action observations in dynamic contexts.     

The hollow-face illusion: object-specific knowledge, general assumptions or properties of the stimulus?

The hollow-face illusion, in which a mask appears as a convex face, is a powerful example of binocular depth inversion occurring with a real object under a wide range of viewing conditions. Explanations of the illusion are reviewed and six experiments reported. In experiment 1 the detrimental effect of figural inversion, evidence for the importance of familiarity, was found for other oriented objects. The inversion effect held for masks lit from the side (experiment 2). The illusion was stronger for a mask rotated by 90 degrees lit from its forehead than from its chin, suggesting that familiar patterns of shading enhance the illusion (experiment 2). There were no effects of light source visibility or any left/right asymmetry (experiment 3). In experiments 4-6 we used a 'virtual' hollow face, with illusion strength quantified by the proportion of noise texture needed to eliminate the illusion. Adding characteristic surface colour enhanced the illusion, consistent with the familiar face pigmentation outweighing additional bottom-up cues (experiment 4). There was no difference between perspective and orthographic projection. Photographic negation reduced, but did not eliminate, the illusion, suggesting shading is important but not essential (experiment 5). Absolute depth was not critical, although a shallower mask was given less extreme convexity ratings (experiment 6). We argue that the illusion arises owing to a convexity preference when the raw data have ambiguous interpretations. However, using a familiar object with typical orientation, shading, and pigmentation greatly enhances the effect.     

The face inversion effect is not a consequence of aberrant eye movements

The face inversion effect is the finding that inverted faces are more difficult to recognize than other inverted objects. The present study explored the possibility that eye movements have a role in producing the face inversion effect. In Experiment 1, we demonstrated that the faces used here produce a robust face inversion effect when compared with another homogenous set of objects (antique radios). In Experiment 2, participants' eye movements were monitored while they learned a set of faces and during a recognition test. Although we clearly found a face inversion effect, the same features of a face were fixated during the learning and recognition test faces, whether the face was right side up or upside down. Thus, the face inversion effect is not a result of a different pattern of eye movements during the viewing of the face.     

Categorization in infancy based on novelty and co-occurrence

Abstract categories (i.e., groups of objects that do not share perceptual features, such as food) abound in everyday situations. The present looking time study investigated whether infants are able to distinguish between two abstract categories (food and toys), and how this ability may extend beyond perceived information by manipulating object familiarity in several ways. Test trials displayed 1) the exact familiarized objects paired as they were during familiarization, 2) a cross-pairing of these same familiar objects, 3) novel objects in the same category as the familiarized items, or 4) novel objects in a different category. Compared to the most familiar test trial (i.e., Familiar Category, Familiar Objects, Familiar Pairings), infants looked longer to all other test trials. Although there was a linear increase in looking time with increased novelty of the test trials (i.e., Novel Category as the most novel test trial), the looking times did not differ significantly between the Novel Category and Familiar Category, Unfamiliar Objects trials. This study contributes to our understanding of how infants form object categories based on object familiarity, object co-occurrence, and information abstraction.     

Drawn towards what others seem to like: Implicit preference for objects and people looked at with a duchenne smile

People tend to like objects that are looked at by others, especially if the person looking at the object expresses a positive emotion. But not all positive emotions are equal. We investigated the effect of third party gazing while expressing subtle positive emotions on perceivers’ subsequent preferences and evaluations of objects and people. In two studies participants saw faces looking at target objects and people either with a Duchenne, a non-Duchenne smile, or a neural expression. Participants first indicated gaze direction and later reported intuitive target preference and evaluated the targets. Results show a preference for target stimuli that were smiled at with a Duchenne smile as opposed to when they were looked at with a non-Duchenne smile or a neutral expression. More explicit evaluations of the target stimuli were not affected by the type of facial expression.     

Representation of the gender of human faces by infants: a preference for female

Six experiments based on visual preference procedures were conducted to examine gender categorization of female versus male faces by infants aged 3 to 4 months. In experiment 1, infants familiarized with male faces preferred a female face over a novel male face, but infants familiarized with female faces divided their attention between a male face and a novel female face. Experiment 2 demonstrated that these asymmetrical categorization results were likely due to a spontaneous preference for females. Experiments 3 and 4 showed that the preference for females was based on processing of the internal facial features in their upright orientation, and not the result of external hair cues or higher-contrast internal facial features. While experiments 1 through 4 were conducted with infants reared with female primary caregivers, experiment 5 provided evidence that infants reared with male primary caregivers tend to show a spontaneous preference for males. Experiment 6 showed that infants reared with female primary caregivers displayed recognition memory for individual females, but not males. These results suggest that representation of information about human faces by young infants may be influenced by the gender of the primary caregiver.     

Individual differences in emotional expression discrimination are associated with emotion label production in toddlers

It is possible that the visual discrimination of emotion categories and emotion word vocabulary develop via common emotion-specific processes. In contrast, it is possible that they develop with vocabulary development more generally. This study contrasts these two possibilities. Twenty-three 26-month-olds participated in a visual perceptual discrimination task involving emotional facial expressions. After familiarization to a 100% happy face, toddlers were tested for their visual preference for a novel sad face in a side-by-side presentation paired with the familiar happy face. Parental report was used to quantify production of emotion words and vocabulary generally. Visual preference for the novel emotion (sad) in the discrimination task correlated with emotion word vocabulary size but not with overall vocabulary size.