Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes

This paper reports on the use of an eye-tracking technique to examine how chimpanzees look at facial photographs of conspecifics. Six chimpanzees viewed a sequence of pictures presented on a monitor while their eye movements were measured by an eye tracker. The pictures presented conspecific faces with open or closed eyes in an upright or inverted orientation in a frame. The results demonstrated that chimpanzees looked at the eyes, nose, and mouth more frequently than would be expected on the basis of random scanning of faces. More specifically, they looked at the eyes longer than they looked at the nose and mouth when photographs of upright faces with open eyes were presented, suggesting that particular attention to the eyes represents a spontaneous face-scanning strategy shared among monkeys, apes, and humans. In contrast to the results obtained for upright faces with open eyes, the viewing times for the eyes, nose, and mouth of inverted faces with open eyes did not differ from one another. The viewing times for the eyes, nose, and mouth of faces with closed eyes did not differ when faces with closed eyes were presented in either an upright or inverted orientation. These results suggest the possibility that open eyes play an important role in the configural processing of faces and that chimpanzees perceive and process open and closed eyes differently.     

I know you are not looking at me: capuchin monkeys’ (<Emphasis Type="Italic">Cebus apella</Emphasis>) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.     

Chimpanzee (Pan troglodytes) intentional communication is not contingent upon food

Studies of great apes have revealed that they use manual gestures and other signals to communicate about distal objects. There is also evidence that chimpanzees modify the types of communicative signals they use depending on the attentional state of a human communicative partner. The majority of previous studies have involved chimpanzees requesting food items from a human experimenter. Here, these same communicative behaviors are reported in chimpanzees requesting a tool from a human observer. In this study, captive chimpanzees were found to gesture, vocalize, and display more often when the experimenter had a tool than when she did not. It was also found that chimpanzees responded differentially based on the attentional state of a human experimenter, and when given the wrong tool persisted in their communicative efforts. Implications for the referential and intentional nature of chimpanzee communicative signaling are discussed.     

Great apes' understanding of other individuals' line of sight

Previous research has shown that many social animals follow the gaze of other individuals. However, knowledge about how this skill differs between species and whether it shows a relationship with genetic distance from humans is still fragmentary. In the present study of gaze following in great apes, we manipulated the nature of a visual obstruction and the presence/absence of a target. We found that bonobos, chimpanzees, and gorillas followed gaze significantly more often when the obstruction had a window than when it did not, just as human infants do. Additionally, bonobos and chimpanzees looked at the experimenter's side of a windowless obstruction more often than the other species. Moreover, bonobos produced more double looks when the barrier was opaque than when it had a window, indicating an understanding of what other individuals see. The most distant human relatives studied, orangutans, showed few signs of understanding what another individual saw. Instead, they were attracted to the target's location by the target's presence, but not by the experimenter's gaze. Great apes' perspective-taking skills seem to have increased in the evolutionary lineage leading to bonobos, chimpanzees, and humans.     

Do chimpanzees tailor their gestural signals to fit the attentional states of others?

The use of vocalizations and tactile gestures by seven juvenile chimpanzees was experimentally investigated. The subjects interacted with an experimenter who typically handed them food rewards. In some trials, however, the experimenter waited 20 s before doing so. In these trials the experimenter’s eyes were either open or closed, or the experimenter was either looking away from the subject or looking directly at him/her inquisitively with head movements. Although the chimpanzees produced at least one of the non-visual gestures mentioned (touching/tapping the experimenter or vocalizing) in 72% of all experimental trials, these actions and vocalizations were deployed without regard to the attentional state of their potential recipient, despite evidence that the subjects noticed the postures that defined the experimenter’s attentional state. The results are discussed in the context of the distinction between the evolution of an understanding of seeing/attention as an internal mental state versus an understanding of behavioral postures alone. Recieved: 12 February 1999 / Accepted after revision: 18 August 1999     

Straight gaze facilitates face processing but does not cause involuntary attentional capture

This study aimed to investigate the conditions under which eyes with a straight gaze capture attention more than eyes with an averted gaze, a phenomenon called the stare-in-the-crowd effect. In Experiment 1, we measured attentional capture by distractor faces with either straight or averted gaze that were shown among faces with closed eyes. Gaze direction of the distractor face was irrelevant because participants searched for a tilted face and indicated its gender. The presence of the distractor face with open eyes resulted in slower reaction times, but gaze direction had no effect, suggesting that straight gaze does not result in more involuntary attentional capture than averted gaze. In three further experiments with the same stimuli, the gaze direction of the target, and not the distractor, was varied. Better performance with straight than averted gaze of the target face was observed when the gaze direction or gender of the target face had to be discriminated. However, no difference between straight and averted was observed when only the presence of a face with open eyes had to be detected. Thus, the stare-in-the crowd effect is only observed when eye gaze is selected as part of the target and only when features of the face have to be discriminated. Our findings suggest that preference for straight gaze bears on target-related processes rather than on attentional capture per se.     

Focus on the essential: all great apes know when others are being attentive

When begging for food, all great ape species are sensitive to a human’s attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216–223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes’ begging behaviour. The authors claimed that while body orientation provides information about the experimenter’s general disposition to offer food, the visibility of the face provides information about the human’s attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216–223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.     

What young children think you see when their eyes are closed

The common assumption that young children egocentrically believe you cannot see them when their own eyes are closed was investigated in two studies. It was found that 2.5-4-year-olds, but not 5-year-olds and adults, would indeed often give negative reply to the experimenter's question “Do I see you?” when their eyes were closed and covered with their hands. However, they would also correctly reply that the experimenter did see their arm and an object placed in front of them and did not see their eyes and back, indicating that they were making veridical, nonegocentric inferences about the experimenter's visual experience. In addition, their eyes being visible to the experimenter did not prove to be either a necessary or a sufficient condition for their judgment that the experimenter could see “them” (“you”). It was concluded that, in this context, adults take “you” to mean their whole body while young children take it to mean primarily their face region. Speculations were made as to how young children could have acquired this meaning, and about possible similarities and differences between the self conceptions of young children and adults.     

What comes first? How selective attentional processes regulate the activation of a motor routine in a manual search task

An intriguing error has been observed in toddlers presented with a 3-location search task involving invisible displacements of an object, namely, the C-not-B task. In 3 experiments, the authors investigated the dynamics of the attentional focus process that is suspected to be involved in this task. In Experiment 1, 2.5-year-old children were tested on a new adaptation of the C-not-B task in which the opening of the experimenter's hand between cloths provided visual information about the correct localization of the toy. Children still emitted a strong response bias toward the last hiding place. In Experiment 2, 2.5-year-old children were tested on a new version of the task that was designed to investigate the role of the central location in the task. This 2nd experiment demonstrated that changing the hand's movement from A to C to B did not enable children to succeed in the task. In Experiment 3, 2.5-year-old children were tested in a situation that is analogous to the C-not-B with open hands task except for the fact that the experimenter dropped the toy under the 1st cloth in the path. Toddlers succeeded when the toy was hidden at Location A but not when it was hidden at Location B. Data indicate that attentional focus on the experimenter's hand motion is contingent on whether that stimulus is critical to performing the task. We argue that these findings provide a potential mechanism through which motor routines can be regulated in accordance with strategic intentions.     

From visual-motor anticipation to conceptualization: Reaction to solid and hollow objects and knowledge of the function of containment

This research investigates the development of visual-manual coordination during infancy with respect to the spatial property of concavity and the development of the capacity to expect or understand that a hollow object affords specific manual behaviors. Tumblers closed at the top by a plexiglas plate were used: They seemed to be open but resisted introduction of the hand. Infants' behavior towards these deceptive objects was compared with their behavior towards identical objects that looked and felt closed or open. The results show that from the 8th month infants exhibit to the deceptive objects an anticipatory visuomotor behavior and from ninth month they exhibit exploratory behavior that suggests that they are trying to understand the discrepancy between the objects' visual and tactile properties. It can therefore be concluded that a rudimentary conceptualization of containment appears to be elaborated by infants from ninth month.     

Blind ethics: Closing one's eyes polarizes moral judgments and discourages dishonest behavior

Four experiments demonstrate that closing one’s eyes affects ethical judgment and behavior because it induces people to mentally simulate events more extensively. People who considered situations with their eyes closed rather than open judged immoral behaviors as more unethical and moral behaviors as more ethical. In addition, considering potential decisions with closed eyes decreased stated intentions to behave ethically and actual self-interested behavior. This relationship was mediated by the more extensive mental simulation that occurred with eyes closed rather than open, which, in turn, intensified emotional reactions to the ethical situation. We discuss the implications of these findings for moral psychology and ethical decision making.     

Body orientation and face orientation: two factors controlling apes’ begging behavior from humans

A number of animal species have evolved the cognitive ability to detect when they are being watched by other individuals. Precisely what kind of information they use to make this determination is unknown. There is particular controversy in the case of the great apes because different studies report conflicting results. In experiment 1, we presented chimpanzees, orangutans, and bonobos with a situation in which they had to request food from a human observer who was in one of various attentional states. She either stared at the ape, faced the ape with her eyes closed, sat with her back towards the ape, or left the room. In experiment 2, we systematically crossed the observers body and face orientation so that the observer could have her body and/or face oriented either towards or away from the subject. Results indicated that apes produced more behaviors when they were being watched. They did this not only on the basis of whether they could see the experimenter as a whole, but they were sensitive to her body and face orientation separately. These results suggest that body and face orientation encode two different types of information. Whereas face orientation encodes the observers perceptual access, body orientation encodes the observers disposition to transfer food. In contrast to the results on body and face orientation, only two of the tested subjects responded to the state of the observers eyes.     

Quantity judgments of auditory and visual stimuli by chimpanzees (Pan troglodytes)

Many species can choose between two visual sets of stimuli on the basis of quantity. This is true when sets are both visible, or are presented one set at a time or even one item at a time. However, we know comparatively little about how well nonhuman animals can compare auditory quantities. Here, three chimpanzees (Pan troglodytes) chose between two sets of food items when they only heard each item fall into different containers rather than seeing those items. This method prevented the chimpanzees from summing the amount of visible food they saw because there were no visual cues. Chimpanzees performed well, and their performance matched that of previous experiments with regard to obeying Weber's law. They also performed well with comparisons between a sequentially presented auditory set and a fully visible set, demonstrating that duration of presentation was not being used as a cue. In addition, they accommodated empty sets into these judgments, although not perfectly. Thus, chimpanzees can judge auditory quantities in flexible ways that show many similarities to how they compare visual quantities.     

Preference for human direct gaze in infant chimpanzees (Pan troglodytes)

We studied gaze perception in three infant chimpanzees (Pan troglodytes), aged 10-32 weeks, using a two-choice preferential-looking paradigm. The infants were presented with two photographs of a human face: (a) with the eyes open or closed, and (b) with a direct or an averted gaze. We found that the chimpanzees preferred looking at the direct-gaze face. However, in the context of scrambled faces, the infants showed no difference in gaze discrimination between direct and averted gazes. These findings suggest that gaze perception by chimpanzees may be influenced by the surrounding facial context. The relationship between gaze perception, face processing, and the adaptive significance of gaze perception are discussed from an evolutionary perspective.     

Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test

Self-directed behaviors (SDBs) are a commonly used behavioral indicator of arousal in nonhuman primates. Experimental manipulations, designed to increase arousal and uncertainty, have been used to elicit SDB production in primates. Beyond measuring rates of SDB production, researchers have also recorded their lateralized production by primates, thought to reflect laterality of hemispheric brain control and response to emotion. Although a handful of such studies exist, all have been conducted with chimpanzees. Expanding on this line of inquiry, we tested both chimpanzees (N = 3) and gorillas (N = 3) in a serial learning task presented on a touchscreen interface that incorporated both EASY (two-item list) and HARD (four-item list) versions of the task. Although SDB production by the apes did not differ across the two levels of task complexity, both species produced higher rates of SDB when they made an error, regardless of task difficulty. Furthermore, the apes made more SDB with the left hand—directed to the right side of their body (contralateral SDB) and left side of their body (ipsilateral SDB)—when they made an incorrect response. There was no difference in the rate of SDB produced with the right hand across correct compared to incorrect trials. The apes’ responses reflect previous reports that show humans are quicker at selecting negative emotional stimuli when using their left, compared to their right, hand (the reverse is true for positive stimuli). However, previous work has shown that chimpanzees are more likely to produce (contralateral) SDB with their right hand when aroused and so we discuss our results in relation to these findings and consider how they relate to the ‘right hemisphere’ and ‘valence’ models of emotional processing in apes.     

Why are you looking at me? It’s because I’m talking,but mostly because I’m staring or not doing much

Our attention is particularly driven toward faces, especially the eyes, and there is much debate over the factors that modulate this social attentional orienting. Most of the previous research has presented faces in isolation, and we tried to address this shortcoming by measuring people’s eye movements whilst they observe more naturalistic and varied social interactions. Participants’ eye movements were monitored whilst they watched three different types of social interactions (monologue, manual activity, active attentional misdirection), which were either accompanied by the corresponding audio as speech or by silence. Our results showed that (1) participants spent more time looking at the face when the person was giving a monologue, than when he/she was carrying out manual activities, and in the latter case they spent more time fixating on the person’s hands. (2) Hearing speech significantly increases the amount of time participants spent looking at the face (this effect was relatively small), although this was not accounted for by any increase in mouth-oriented gaze. (3) Participants spent significantly more time fixating on the face when direct eye contact was established, and this drive to establish eye contact was significantly stronger in the manual activities than during the monologue. These results highlight people’s strategic top-down control over when they attend to faces and the eyes, and support the view that we use our eyes to signal non-verbal information.     

On the functional role of the verbalization in correspondence training procedures

We investigated the functional role of the child's and experimenter's verbalizations in correspondence training procedures with toy play behaviors in a day-care center setting. Six children participated in a multiple baseline across responses and/or multielement design. Baseline conditions were followed by reinforcement of verbalization. This resulted in little or no change in responding, similar to findings of previous research. Experiment I isolated the child's verbalization as the variable under study. With an experimenter's prompt and postplay reinforcement held constant, the effects of including versus omitting the child's verbalization were examined. A contingency-space analysis revealed that the presence or absence of the child's verbalization exerted no influence on play with the target toy. In Experiment II, a condition in which no experimenter's prompt occurred was added. Results suggested that the complete absence of any antecedent verbalization, by child or experimenter, resulted in much lower rates of play with the target toys. Again, however, when the experimenter's prompt was included, no clear difference was noted between conditions in which the child verbalized and conditions in which the child did not. These results raise doubts about the commonly held view of correspondence training procedures as a method of promoting self-regulation.     

When one sees what the other hears: Crossmodal attentional modulation for gazed and non-gazed upon auditory targets

Three experiments investigated the nature of visuo-auditory crossmodal cueing in a triadic setting: participants had to detect an auditory signal while observing another agent’s head facing one of the two laterally positioned auditory sources. Experiment 1 showed that when the agent’s eyes were open, sounds originating on the side of the agent’s gaze were detected faster than sounds originating on the side of the agent’s visible ear; when the agent’s eyes were closed this pat-tern of responses was reversed. Two additional experiments showed that the results were sensitive to whether participants could infer a hearing function on the part of the agent. When no ear was depicted on the agent, only a gaze-side advantage was observed (Experiment 2), but when the agent’s ear was covered (Experiment 3), an ear side advantage was observed only when hearing could still be inferred (i.e., wearing the hat) but not when hearing was inferred to be diminished (i.e., wearing a helmet). The findings are discussed in the context of inferential and simulation processes and joint attention mechanisms.     

Selfish strategies develop in social problem situations in chimpanzee (Pan troglodytes) mother–infant pairs

Humans employ various strategies, including selfish and altruistic strategies, depending on the situation. In order to examine whether non-human animals show such flexibility or not, we analyzed chimpanzees’ selfish and cooperative behavior in two types of social problem situations. In this study, we tested chimpanzee mother–infant pairs in two adjacent booths, each equipped with a vending machine. When a token was inserted into a vending machine, the vending machine delivered food rewards to the adjacent booth. In experiment 1, a partition between the two booths was open. In experiment 2, the partition was closed and a mother and her infant were placed in separate booths, so that reciprocal cooperation was essential for them to receive rewards. The participants did not cooperate reciprocally in either experiment. In experiment 1, the chimpanzees developed selfish tactics to get rewards and changed their tactics flexibly according to the partner’s behaviors. In experiment 2, in which they could not receive rewards without cooperation, they stopped altogether inserting tokens. In both cases, the infants stopped cooperating first. These findings support the idea that chimpanzees are primarily competitive rather than cooperative. Chimpanzees’ high social intelligence might be demonstrated in the flexibility of their selfish tactics, but not in the form of reciprocal cooperation at least when food is involved. We suggest that the failure to establish reciprocal cooperation was due to the social relationship between the mother and her infant, which was characterized by infant’s privilege and mother’s tolerance.     

Different step-over movement strategies for disturbance stimulations

This study examined differences in performance when 10 healthy adult participants took steps under three different disturbance stimulations (with opened and closed eyes and with the use of light), with and without an obstacle present. In the voluntary condition, participants recognized the obstacle beforehand and stepped over it quickly; in the light condition, participants recognized the obstacle beforehand and quickly stepped over it after light stimulation; in the closed eyes condition, participants did not recognize the obstacle beforehand, but after opening their eyes when hearing a sound, they quickly stepped over the obstacle. The swing time of the gait was significantly longer in obstacle conditions for all stimulations. The swing time was significantly longer under the closed eyes condition than the light and voluntary conditions. The clearances were significantly higher in order of the closed eyes, light, and voluntary conditions in the presence of an obstacle.