Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis

As compared with other primates, humans have especially visible eyes (e.g., white sclera). One hypothesis is that this feature of human eyes evolved to make it easier for conspecifics to follow an individual's gaze direction in close-range joint attentional and communicative interactions, which would seem to imply especially cooperative (mututalistic) conspecifics. In the current study, we tested one aspect of this cooperative eye hypothesis by comparing the gaze following behavior of great apes to that of human infants. A human experimenter "looked" to the ceiling either with his eyes only, head only (eyes closed), both head and eyes, or neither. Great apes followed gaze to the ceiling based mainly on the human's head direction (although eye direction played some role as well). In contrast, human infants relied almost exclusively on eye direction in these same situations. These results demonstrate that humans are especially reliant on eyes in gaze following situations, and thus, suggest that eyes evolved a new social function in human evolution, most likely to support cooperative (mututalistic) social interactions.     

Patterns of Gazing in Orangutans (Pongo pygmaeus)

Eyes play an important role in communication amongst humans and animals. However, relatively little is known about specific differences in eye morphology amongst primates and how these features might be associated with social structure and direction of gaze. We present a detailed study of gazing and eye morphology—exposed sclera and surrounding features—in orangutans. We measured gazing in rehabilitating orangutans in two contexts: interspecific viewing of the experimenter (with video camera) and intraspecific gazing (between subjects). Our findings show that direct staring is avoided and social looking is limited to certain age/social categories: juveniles engage in more looking at other orangutans than do adults or infants. While orangutans use eye movements in social communication, they avoid the more prolonged mutual gaze that is characteristic of humans, and also apparent in chimpanzees and gorillas. Detailed frame-by-frame analysis of videotapes from field and zoo studies of orangutans revealed that they pay visual attention to both human observers and conspecifics by glancing sideways, with the head turned at an angle away from the subject being observed. Mutual gaze was extremely rare, and we have observed only two incidences of gaze following. Orangutans in captivity appear to use a more restricted pattern of gazes compared to free-living, rehabilitating ones, possibly suggesting the presence of a pathological condition (such as depression) in the captive subjects. Our findings have implications for further investigations of social communication and cognition in orangutans.     

Do American Crows Pay Attention to Human Gaze and Facial Expressions?

Interactions between species can lead to the evolution of interspecific communication. Non‐verbal communication by humans, both intentional and unintentional, can be interpreted by other species. We tested whether American crows (Corvus brachyrhynchos) were sensitive to human facial features under field conditions by comparing flight initiation distances and urgency of escape behavior to human approaches varying in eye contact and facial expression. We first examined whether crows distinguish between an approaching human who is directly gazing at them and a human approaching them with an averted gaze. In a second experiment, we tested whether crows differentiate a smiling from scowling human approaching them with direct or averted gaze. In the first experiment, we found that crows fled sooner and more urgently when humans were directly gazing at them. Similarly, in the second experiment, crows responded sooner to a direct vs. averted gaze; however, they did not react differently to varying human facial expressions. We suggest that crows use human gaze as a reliable visual cue compared with facial expressions when making decisions about responding to approaching humans. This is the first study to show that a wild corvid species changes its behavior based on human gaze, possibly representing an adaptation to living in human‐dominated urban areas and suggesting crows might perceive human intention by this visual cue.     

Visual Search for Human Gaze Direction by a Chimpanzee (Pan troglodytes)

Background

Humans detect faces with direct gazes among those with averted gazes more efficiently than they detect faces with averted gazes among those with direct gazes. We examined whether this “stare-in-the-crowd” effect occurs in chimpanzees (Pan troglodytes), whose eye morphology differs from that of humans (i.e., low-contrast eyes, dark sclera).

Methodology/Principal Findings

An adult female chimpanzee was trained to search for an odd-item target (front view of a human face) among distractors that differed from the target only with respect to the direction of the eye gaze. During visual-search testing, she performed more efficiently when the target was a direct-gaze face than when it was an averted-gaze face. This direct-gaze superiority was maintained when the faces were inverted and when parts of the face were scrambled. Subsequent tests revealed that gaze perception in the chimpanzee was controlled by the contrast between iris and sclera, as in humans, but that the chimpanzee attended only to the position of the iris in the eye, irrespective of head direction.

Conclusion/Significance

These results suggest that the chimpanzee can discriminate among human gaze directions and are more sensitive to direct gazes. However, limitations in the perception of human gaze by the chimpanzee are suggested by her inability to completely transfer her performance to faces showing a three-quarter view.     

Salient eyes deter conspecific nest intruders in wild jackdaws (Corvus monedula)

Animals often respond fearfully when encountering eyes or eye-like shapes. Although gaze aversion has been documented in mammals when avoiding group-member conflict, the importance of eye coloration during interactions between conspecifics has yet to be examined in non-primate species. Jackdaws (Corvus monedula) have near-white irides, which are conspicuous against their dark feathers and visible when seen from outside the cavities where they nest. Because jackdaws compete for nest sites, their conspicuous eyes may act as a warning signal to indicate that a nest is occupied and deter intrusions by conspecifics. We tested whether jackdaws’ pale irides serve as a deterrent to prospecting conspecifics by comparing prospectors’ behaviour towards nest-boxes displaying images with bright eyes (BEs) only, a jackdaw face with natural BEs, or a jackdaw face with dark eyes. The jackdaw face with BEs was most effective in deterring birds from making contact with nest-boxes, whereas both BE conditions reduced the amount of time jackdaws spent in proximity to the image. We suggest BEs in jackdaws may function to prevent conspecific competitors from approaching occupied nest sites.     

Cultural Modulation of Face and Gaze Scanning in Young Children

Previous research has demonstrated that the way human adults look at others’ faces is modulated by their cultural background, but very little is known about how such a culture-specific pattern of face gaze develops. The current study investigated the role of cultural background on the development of face scanning in young children between the ages of 1 and 7 years, and its modulation by the eye gaze direction of the face. British and Japanese participants’ eye movements were recorded while they observed faces moving their eyes towards or away from the participants. British children fixated more on the mouth whereas Japanese children fixated more on the eyes, replicating the results with adult participants. No cultural differences were observed in the differential responses to direct and averted gaze. The results suggest that different patterns of face scanning exist between different cultures from the first years of life, but differential scanning of direct and averted gaze associated with different cultural norms develop later in life.     

Speaking and Listening with the Eyes: Gaze Signaling during Dyadic Interactions

Cognitive scientists have long been interested in the role that eye gaze plays in social interactions. Previous research suggests that gaze acts as a signaling mechanism and can be used to control turn-taking behaviour. However, early research on this topic employed methods of analysis that aggregated gaze information across an entire trial (or trials), which masks any temporal dynamics that may exist in social interactions. More recently, attempts have been made to understand the temporal characteristics of social gaze but little research has been conducted in a natural setting with two interacting participants. The present study combines a temporally sensitive analysis technique with modern eye tracking technology to 1) validate the overall results from earlier aggregated analyses and 2) provide insight into the specific moment-to-moment temporal characteristics of turn-taking behaviour in a natural setting. Dyads played two social guessing games (20 Questions and Heads Up) while their eyes were tracked. Our general results are in line with past aggregated data, and using cross-correlational analysis on the specific gaze and speech signals of both participants we found that 1) speakers end their turn with direct gaze at the listener and 2) the listener in turn begins to speak with averted gaze. Convergent with theoretical models of social interaction, our data suggest that eye gaze can be used to signal both the end and the beginning of a speaking turn during a social interaction. The present study offers insight into the temporal dynamics of live dyadic interactions and also provides a new method of analysis for eye gaze data when temporal relationships are of interest.     

Kangaroos display gazing and gaze alternations during an unsolvable problem task

Domestication is generally assumed to have resulted in enhanced communication abilities between non-primate mammals and humans, although the number of species studied is very limited (e.g. cats, Felis catus; dogs, Canis familiaris; wolves, Canis lupus; goats, Capra hircus; horses, Equus caballus). In species without hands for pointing, gazing at humans when dealing with inaccessible food during an unsolvable task, and in particular gaze alternations between a human and the unsolvable task (considered forms of showing), are often interpreted as attempts at referential intentional communication. We report that kangaroos, marsupial mammals that have never been domesticated, actively gazed at an experimenter during an unsolvable problem task (10/11 kangaroos tested), thus challenging the notion that this behaviour results from domestication. Nine of the 10 kangaroos additionally showed gaze alternations between the unsolvable task and experimenter. We propose that the potential occurrence of these behaviours displayed towards humans has been underestimated, owing to a narrow focus on domestic animals, as well as a more general eutherian research bias.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Gaze following in human infants depends on communicative signals

Humans are extremely sensitive to ostensive signals, like eye contact or having their name called, that indicate someone's communicative intention toward them [1-3]. Infants also pay attention to these signals [4-6], but it is unknown whether they appreciate their significance in the initiation of communicative acts. In two experiments, we employed video presentation of an actor turning toward one of two objects and recorded infants' gaze-following behavior [7-13] with eye-tracking techniques [11, 12]. We found that 6-month-old infants followed the adult's gaze (a potential communicative-referential signal) toward an object only when such an act is preceded by ostensive cues such as direct gaze (experiment 1) and infant-directed speech (experiment 2). Such a link between the presence of ostensive signals and gaze following suggests that this behavior serves a functional role in assisting infants to effectively respond to referential communication directed to them. Whereas gaze following in many nonhuman species supports social information gathering [14-18], in humans it initially appears to reflect the expectation of a more active, communicative role from the information source.     

Chimpanzees and Humans Mimic Pupil-Size of Conspecifics

Group-living typically provides benefits to individual group members but also confers costs. To avoid incredulity and betrayal and allow trust and cooperation, individuals must understand the intentions and emotions of their group members. Humans attend to other''s eyes and from gaze and pupil-size cues, infer information about the state of mind of the observed. In humans, pupil-size tends to mimic that of the observed. Here we tested whether pupil-mimicry exists in our closest relative, the chimpanzee (P. troglodytes). We conjectured that if pupil-mimicry has adaptive value, e.g. to promote swift communication of inner states and facilitate shared understanding and coordination, pupil-mimicry should emerge within but not across species. Pupillometry data was collected from human and chimpanzee subjects while they observed images of the eyes of both species with dilating/constricting pupils. Both species showed enhanced pupil-mimicry with members of their own species, with effects being strongest in humans and chimpanzee mothers. Pupil-mimicry may be deeply-rooted, but probably gained importance from the point in human evolution where the morphology of our eyes became more prominent. Humans'' white sclera surrounding the iris, and the fine muscles around their eyes facilitate non-verbal communication via eye signals.     

A simple reason for a big difference: wolves do not look back at humans,but dogs do

The present investigations were undertaken to compare interspecific communicative abilities of dogs and wolves, which were socialized to humans at comparable levels. The first study demonstrated that socialized wolves were able to locate the place of hidden food indicated by the touching and, to some extent, pointing cues provided by the familiar human experimenter, but their performance remained inferior to that of dogs. In the second study, we have found that, after undergoing training to solve a simple manipulation task, dogs that are faced with an insoluble version of the same problem look/gaze at the human, while socialized wolves do not. Based on these observations, we suggest that the key difference between dog and wolf behavior is the dogs' ability to look at the human's face. Since looking behavior has an important function in initializing and maintaining communicative interaction in human communication systems, we suppose that by positive feedback processes (both evolutionary and ontogenetically) the readiness of dogs to look at the human face has lead to complex forms of dog-human communication that cannot be achieved in wolves even after extended socialization.     

Chimpanzees (Pan troglodytes) Produce the Same Types of ‘Laugh Faces’ when They Emit Laughter and when They Are Silent

The ability to flexibly produce facial expressions and vocalizations has a strong impact on the way humans communicate, as it promotes more explicit and versatile forms of communication. Whereas facial expressions and vocalizations are unarguably closely linked in primates, the extent to which these expressions can be produced independently in nonhuman primates is unknown. The present work, thus, examined if chimpanzees produce the same types of facial expressions with and without accompanying vocalizations, as do humans. Forty-six chimpanzees (Pan troglodytes) were video-recorded during spontaneous play with conspecifics at the Chimfunshi Wildlife Orphanage. ChimpFACS was applied, a standardized coding system to measure chimpanzee facial movements, based on FACS developed for humans. Data showed that the chimpanzees produced the same 14 configurations of open-mouth faces when laugh sounds were present and when they were absent. Chimpanzees, thus, produce these facial expressions flexibly without being morphologically constrained by the accompanying vocalizations. Furthermore, the data indicated that the facial expression plus vocalization and the facial expression alone were used differently in social play, i.e., when in physical contact with the playmates and when matching the playmates’ open-mouth faces. These findings provide empirical evidence that chimpanzees produce distinctive facial expressions independently from a vocalization, and that their multimodal use affects communicative meaning, important traits for a more explicit and versatile way of communication. As it is still uncertain how human laugh faces evolved, the ChimpFACS data were also used to empirically examine the evolutionary relation between open-mouth faces with laugh sounds of chimpanzees and laugh faces of humans. The ChimpFACS results revealed that laugh faces of humans must have gradually emerged from laughing open-mouth faces of ancestral apes. This work examines the main evolutionary changes of laugh faces since the last common ancestor of chimpanzees and humans.     

Attention to Eye Contact in the West and East: Autonomic Responses and Evaluative Ratings

Eye contact has a fundamental role in human social interaction. The special appearance of the human eye (i.e., white sclera contrasted with a coloured iris) implies the importance of detecting another person''s face through eye contact. Empirical studies have demonstrated that faces making eye contact are detected quickly and processed preferentially (i.e., the eye contact effect). Such sensitivity to eye contact seems to be innate and universal among humans; however, several studies suggest that cultural norms affect eye contact behaviours. For example, Japanese individuals exhibit less eye contact than do individuals from Western European or North American cultures. However, how culture modulates eye contact behaviour is unclear. The present study investigated cultural differences in autonomic correlates of attentional orienting (i.e., heart rate) and looking time. Additionally, we examined evaluative ratings of eye contact with another real person, displaying an emotionally neutral expression, between participants from Western European (Finnish) and East Asian (Japanese) cultures. Our results showed that eye contact elicited stronger heart rate deceleration responses (i.e., attentional orienting), shorter looking times, and higher ratings of subjective feelings of arousal as compared to averted gaze in both cultures. Instead, cultural differences in the eye contact effect were observed in various evaluative responses regarding the stimulus faces (e.g., facial emotion, approachability etc.). The rating results suggest that individuals from an East Asian culture perceive another''s face as being angrier, unapproachable, and unpleasant when making eye contact as compared to individuals from a Western European culture. The rating results also revealed that gaze direction (direct vs. averted) could influence perceptions about another person''s facial affect and disposition. These results suggest that cultural differences in eye contact behaviour emerge from differential display rules and cultural norms, as opposed to culture affecting eye contact behaviour directly at the physiological level.     

Mimicry of food intake: the dynamic interplay between eating companions

Numerous studies have shown that people adjust their intake directly to that of their eating companions; they eat more when others eat more, and less when others inhibit intake. A potential explanation for this modeling effect is that both eating companions'' food intake becomes synchronized through processes of behavioral mimicry. No study, however, has tested whether behavioral mimicry can partially account for this modeling effect. To capture behavioral mimicry, real-time observations of dyads of young females having an evening meal were conducted. It was assessed whether mimicry depended on the time of the interaction and on the person who took the bite. A total of 70 young female dyads took part in the study, from which the total number of bites (N = 3,888) was used as unit of analyses. For each dyad, the total number of bites and the exact time at which each person took a bite were coded. Behavioral mimicry was operationalized as a bite taken within a fixed 5-second interval after the other person had taken a bite, whereas non-mimicked bites were defined as bites taken outside the 5-second interval. It was found that both women mimicked each other''s eating behavior. They were more likely to take a bite of their meal in congruence with their eating companion rather than eating at their own pace. This behavioral mimicry was found to be more prominent at the beginning than at the end of the interaction. This study suggests that behavioral mimicry may partially account for social modeling of food intake.     

Reflexive social attention in monkeys and humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.     

Putting Culture Under the ‘Spotlight’ Reveals Universal Information Use for Face Recognition

Background

Eye movement strategies employed by humans to identify conspecifics are not universal. Westerners predominantly fixate the eyes during face recognition, whereas Easterners more the nose region, yet recognition accuracy is comparable. However, natural fixations do not unequivocally represent information extraction. So the question of whether humans universally use identical facial information to recognize faces remains unresolved.

Methodology/Principal Findings

We monitored eye movements during face recognition of Western Caucasian (WC) and East Asian (EA) observers with a novel technique in face recognition that parametrically restricts information outside central vision. We used ‘Spotlights’ with Gaussian apertures of 2°, 5° or 8° dynamically centered on observers'' fixations. Strikingly, in constrained Spotlight conditions (2° and 5°) observers of both cultures actively fixated the same facial information: the eyes and mouth. When information from both eyes and mouth was simultaneously available when fixating the nose (8°), as expected EA observers shifted their fixations towards this region.

Conclusions/Significance

Social experience and cultural factors shape the strategies used to extract information from faces, but these results suggest that external forces do not modulate information use. Human beings rely on identical facial information to recognize conspecifics, a universal law that might be dictated by the evolutionary constraints of nature and not nurture.     

What is unique about the human eye? Comparative image analysis on the external eye morphology of human and nonhuman great apes

The gaze-signaling hypothesis and the related cooperative-eye hypothesis posit that humans have evolved special external eye morphology, including exposed white sclera (the white of the eye), to enhance the visibility of eye-gaze direction and thereby facilitate conspecific communication through joint-attentional interaction and ostensive communication. However, recent quantitative studies questioned these hypotheses based on new findings that certain features of human eyes are not necessarily unique among great ape species. Accordingly, there is currently a heated debate over whether external eye features of humans are distinct from those of other apes and how such distinguishable features contribute to the visibility of eye-gaze direction. The present study leveraged updated image analysis techniques to test the uniqueness of human eye features in facial images of great apes. Although many eye features were similar between humans and other great apes, a key difference was that humans have uniformly white sclera which creates clear visibility of both the eye outline and iris—the two essential features contributing to the visibility of eye-gaze direction. We then tested the robustness of the visibility of these features against visual noise, such as shading and distancing, and found that both eye features remain detectable in the human eye, while eye outline becomes barely detectable in other species under these visually challenging conditions. Overall, we identified that humans have unique external eye morphology among other great apes, which ensures the robustness of eye-gaze signals in various visual conditions. Our results support and also critically update the central premises of the gaze-signaling hypothesis.     

Do more sociable dogs gaze longer to the human face than less sociable ones?

Domestic dogs (Canis familiaris) are especially skillful in communicating with humans, and they rely on special abilities to do that. One of these skills involves gazing at human faces in cases of uncertainty or when seeking for something out of reach. In this study, we evaluated the relationship between dogs' sociability level and the ability to learn to gaze in a situation with food in sight but out of their reach. Thirty-nine adult dogs were tested in two procedures: (1) a sociability test that involved interacting with an unknown person, and (2) a learning task that consisted of training trials in which gazing at the experimenter's face was food reinforced, followed by extinction trials in which gazing was not followed by food. A significant positive correlation was found between the duration of physical contact with the unknown person in the sociability test and gaze duration during extinction. Moreover, high sociability dogs gazed significantly longer at humans during extinction trials. We discuss the possibility that, more sociable animals, such as those who pay more attention to the person in our sociability test, may be more persistent in their communicative attempts because the presence of the human is intrinsically reinforcing to them. Finally, we comment on the importance of these findings for training purposes.     

Dealing with Target Uncertainty in a Reaching Control Interface

Prosthetic devices need to be controlled by their users, typically using physiological signals. People tend to look at objects before reaching for them and we have shown that combining eye movements with other continuous physiological signal sources enhances control. This approach suffers when subjects also look at non-targets, a problem we addressed with a probabilistic mixture over targets where subject gaze information is used to identify target candidates. However, this approach would be ineffective if a user wanted to move towards targets that have not been foveated. Here we evaluated how the accuracy of prior target information influenced decoding accuracy, as the availability of neural control signals was varied. We also considered a mixture model where we assumed that the target may be foveated or, alternatively, that the target may not be foveated. We tested the accuracy of the models at decoding natural reaching data, and also in a closed-loop robot-assisted reaching task. The mixture model worked well in the face of high target uncertainty. Furthermore, errors due to inaccurate target information were reduced by including a generic model that relied on neural signals only.