Use of experimenter-given cues in visual co-orienting and in an object-choice task by a new world monkey species, cotton top tamarins (Saguinus oedipus)

Two methods assessed the use of experimenter-given directional cues by a New World monkey species, cotton top tamarins (Saguinus oedipus). Experiment 1 used cues to elicit visual co-orienting toward distal objects. Experiment 2 used cues to generate responses in an object-choice task. Although there were strong positive correlations between monkey pairs to co-orient, visual co-orienting with a human experimenter occurred at a low frequency to distal objects. Human hand pointing cues generated more visual co-orienting than did eye gaze to distal objects. Significant accurate choices of baited cups occurred with human point and tap cues and human look cues. Results highlight the importance of head and body orientation to induce shared attention in cotton top tamarins, both in a task that involved food getting and a task that did not.     

Nonenculturated orangutans' (Pongo pygmaeus) use of experimenter-given manual and facial cues in an object-choice task

Several experiments have been performed, to examine whether nonhuman primates are able to make use of experimenter-given manual and facial (visual) cues to direct their attention to a baited object. Contrary to the performance of prosimians and monkeys, great apes repeatedly have shown task efficiency in experiments such as these. However, many great ape subjects used have been "enculturated" individuals. In the present study, 3 nonenculturated orangutans (Pongo pygmaeus) were tested for their ability to use experimenter-given pointing, gazing, and glancing cues in an object-choice task. All subjects readily made use of the pointing gesture. However, when subjects were left with only gazing or glancing cues, their performance deteriorated markedly, and they were not able to complete the task.     

An infant chimpanzee (Pan troglodytes) follows human gaze

The ability of non-human primates to follow the gaze of other individuals has recently received much attention in comparative cognition. The aim of the present study was to investigate the emergence of this ability in a chimpanzee infant. The infant was trained to look at one of two objects, which an experimenter indicated by one of four different cue conditions: (1) tapping on the target object with a finger; (2) pointing to the target object with a finger; (3) gazing at the target object with head orientation; or (4) glancing at the target object without head orientation. The subject was given food rewards independently of its responses under the first three conditions, so that its responses to the objects were not influenced by the rewards. The glancing condition was tested occasionally, without any reinforcement. By the age of 13 months, the subject showed reliable following responses to the object that was indicated by the various cues, including glancing alone. Furthermore, additional tests clearly showed that the subject's performance was controlled by the "social" properties of the experimenter-given cues but not by the non-social, local-enhancing peripheral properties. Electronic Publication     

Development of using experimenter-given cues in infant chimpanzees: longitudinal changes in behavior and cognitive development

The use of gaze shifts as social cues has various evolutionary advantages. To investigate the developmental processes of this ability, we conducted an object-choice task by using longitudinal methods with infant chimpanzees tested from 8 months old until 3 years old. The experimenter used one of six gestures towards a cup concealing food; tapping, touching, whole-hand pointing, gazing plus close-pointing, distant-pointing, close-gazing, and distant-gazing. Unlike any other previous study, we analyzed the behavioral changes that occurred before and after choosing the cup. We assumed that pre-choice behavior indicates the development of an attentional and spatial connection between a pointing cue and an object (e.g. Woodward, 2005); and post-choice behavior indicates the emergence of object permanence (e.g. Piaget, 1954). Our study demonstrated that infant chimpanzees begin to use experimenter-given cues with age (after 11 months of age). Moreover, the results from the behavioral analysis showed that the infants gradually developed the spatial link between the pointing as an object-directed action and the object. Moreover, when they were 11 months old, the infants began to inspect the inside of the cup, suggesting the onset of object permanence. Overall, our results imply that the ability to use the cues is developing and mutually related with other cognitive developments. The present study also suggests what the standard object-choice task actually measures by breaking the task down into the developmental trajectories of its component parts, and describes for the first time the social-physical cognitive development during the task with a longitudinal method.     

Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task

The ability of 3 capuchin monkeys (Cebus apella) to use experimenter-given cues to solve an object-choice task was assessed. The monkeys learned to use explicit gestural and postural cues and then progressed to using eye-gaze-only cues to solve the task, that is, to choose the baited 1 of 2 objects and thus obtain a food reward. Increasing cue-stimulus distance and introducing movement of the eyes impeded the establishment of effective eye-gaze reading. One monkey showed positive but imperfect transfer of use of eye gaze when a novel experimenter presented the cue. When head and eye orientation cues were presented simultaneously and in conflict, the monkeys showed greater responsiveness to head orientation cues. The results show that capuchin monkeys can learn to use eye gaze as a discriminative cue, but there was no-evidence for any underlying awareness of eye gaze as a cue to direction of attention.     

Comprehension of human pointing gestures in horses (Equus caballus)

Twenty domestic horses (Equus caballus) were tested for their ability to rely on different human gesticular cues in a two-way object choice task. An experimenter hid food under one of two bowls and after baiting, indicated the location of the food to the subjects by using one of four different cues. Horses could locate the hidden reward on the basis of the distal dynamic-sustained, proximal momentary and proximal dynamic-sustained pointing gestures but failed to perform above chance level when the experimenter performed a distal momentary pointing gesture. The results revealed that horses could rely spontaneously on those cues that could have a stimulus or local enhancement effect, but the possible comprehension of the distal momentary pointing remained unclear. The results are discussed with reference to the involvement of various factors such as predisposition to read human visual cues, the effect of domestication and extensive social experience and the nature of the gesture used by the experimenter in comparative investigations.     

Comprehension of human pointing gestures in young human-reared wolves (<Emphasis Type="Italic">Canis lupus</Emphasis>) and dogs (<Emphasis Type="Italic">Canis familiaris</Emphasis>)

Dogs have a remarkable skill to use human-given cues in object-choice tasks, but little is known to what extent their closest wild-living relative, the wolf can achieve this performance. In Study 1, we compared wolf and dog pups hand-reared individually and pet dogs of the same age in their readiness to form eye-contact with a human experimenter in an object-choice task and to follow her pointing gesture. The results showed that dogs already at 4 months of age use momentary distal pointing to find hidden food even without intensive early socialization. Wolf pups, on the contrary, do not attend to this subtle pointing. Accordingly in Studies 2 and 3, these wolves were tested longitudinally with this and four other (easier) human-given cues. This revealed that wolves socialized at a comparable level to dogs are able to use simple human-given cues spontaneously if the human’s hand is close to the baited container (e.g. touching, proximal pointing). Study 4 showed that wolves can follow also momentary distal pointing similarly to dogs if they have received extensive formal training. Comparing the wolves to naïve pet dogs of the same age revealed that during several months of formal training wolves can reach the level of dogs in their success of following momentary distal pointing in parallel with improving their readiness to form eye-contact with a human experimenter. We assume that the high variability in the wolves’ communicative behaviour might have provided a basis for selection during the course of domestication of the dog.     

Behavioral cues that great apes use to forage for hidden food

We conducted three studies to examine whether the four great ape species (chimpanzees, bonobos, gorillas, and orangutans) are able to use behavioral experimenter-given cues in an object-choice task. In the subsequent experimental conditions subjects were presented with two eggs, one of which contained food and the other did not. In Study 1 the experimenter examined both eggs by smelling or shaking them, but only made a failed attempt to open (via biting) the egg containing food. In a control condition, the experimenter examined and attempted to open both eggs, but in reverse order to control for stimulus enhancement. The apes significantly preferred the egg that was first examined and then bitten, but had no preference in a baseline condition in which there were no cues. In Study 2, we investigated whether the apes could extend this ability to cues not observed in apes so far (i.e., attempting to pull apart the egg), as well as whether they made this discrimination based on the function of the action the experimenter performed. Subjects significantly preferred eggs presented with this novel cue, but did not prefer eggs presented with a novel but functionally irrelevant action. In Study 3, apes did not interpret human actions as cues to food-location when they already knew that the eggs were empty. Thus, great apes were able to use a variety of experimenter-given cues associated with foraging actions to locate hidden food and thereby were partially sensitive to the general purpose underlying these actions.     

Do common ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>) rely on human or conspecific gaze cues to detect hidden food?

The ability of non-human animals to use experimenter-given cues in object-choice tasks has recently gained interest. In such experiments, the location of hidden food is indicated by an experimenter, e.g. by gazing, pointing or touching. Whereas dogs apparently outperform all other species so far tested, apes and monkeys have problems in using such cues. Since only mammalian species have been tested, information is lacking about the evolutionary origin of these abilities. We here present the first data on object-choice tasks conducted with an avian species, the common raven. Ravens are highly competitive scavengers, possessing sophisticated cognitive skills in protecting their food caches and pilfering others’ caches. We conducted three experiments, exploring (i) which kind of cues ravens use for choosing a certain object, (ii) whether ravens use humans’ gaze for detecting hidden food and (iii) whether ravens would find hidden food in the presence of an informed conspecific who potentially provides gaze cues. Our results indicate that ravens reliably respond to humans’ touching of an object, but they hardly use point and gaze cues for their choices. Likewise, they do not perform above chance level in the presence of an informed conspecific. These findings mirror those obtained for primates and suggest that, although ravens may be aware of the gaze direction of humans and conspecifics, they apparently do not rely on this information to detect hidden food.     

Juvenile domestic pigs (Sus scrofa domestica) use human-given cues in an object choice task

Research on the comprehension of human-given cues by domesticated as well as non-domesticated species has received considerable attention over the last decade. While several species seem to be capable of utilizing these cues, former work with domestic pigs (Sus scrofa domestica) has shown inconclusive results. In this study, we investigated the use of human-given cues in an object choice task by young domestic pigs (N = 17; 7 weeks of age) who had very limited human contact prior to the experiments. Subjects had to choose between two bowls of which only one was baited with a reward. Over the course of five experiments, pigs were able to use proximal and, with some constraints, also distal pointing cues presented in both a dynamic-sustained and in a momentary manner. When the experimenter was pointing from the incorrect bowl towards the correct one, most of the subjects had problems solving the task—indicating that some form of stimulus/local enhancement affected pigs’ decision making. Interestingly, pigs were able to utilize the body and head orientation of a human experimenter to locate the hidden reward but failed to co-orient when head or body orientation of the experimenter was directed into distant space with no bowls present. Control trials ruled out the possibility that other factors (e.g. odour cues) affected subjects’ choice behaviour. Learning during experiments played a minor role and only occurred in three out of twelve test conditions. We conclude that domestic pigs, even at a very young age, are skilful in utilizing various human-given cues in an object choice task—raising the question whether pigs only used stimulus/local enhancement and associative learning processes or whether they were able to comprehend the communicative nature of at least some of these cues.     

Conflicting Social Cues: Fourteen- and 24-Month-Old Infants' Reliance on Gaze and Pointing Cues in Word Learning

Language acquisition is a process embedded in social routines. Despite considerable attention in research to its social nature, little is known about developmental differences in the relative priority of certain social cues over others during early word learning. Employing an eye-tracking paradigm, we presented 14-month-old infants, 24-month-old infants, and adults with movies in which an actor repeatedly gazed at one and pointed to the other of two objects while presenting them with a novel word. The results show that the 14-month-old infants pay more attention to a model's eye gaze when learning to map a novel word to a referent, whereas 24-month-old infants and adults rely more on pointing cues. Our results provide evidence for a developmental change in the relative priority of pointing versus eye-gazing cues in language acquisition.     

Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus)

Sixteen domestic dogs (Canis familiaris) and four horses (Equus caballus) were tested for their ability to use human-given manual and facial cues in an object-choice task. Two of the four horses used touch as a cue and one horse successfully used pointing. The performance of the dogs was considerably better, with 12 subjects able to use pointing as a cue, 4 able to use head orientation and 2 able to use eye gaze alone. Group analysis showed that the dogs performed significantly better in all experimental conditions than during control trials. Dogs were able to use pointing cues even when the cuer’s body was closer to the incorrect object. Working gundogs with specialised training used pointing more successfully than pet dogs and gundog breeds performed better than non-gundog breeds. The results of this experiment suggest that animals’ use of human given communicative signals depends on cognitive ability, the evolutionary consequences of domestication and enculturation by humans within the individual’s lifetime. Received: 15 July 1999 / Accepted after revision: 10 January 2000     

Chimpanzee Use of Human and Conspecific Social Cues to Locate Hidden Food

Two studies are reported in which chimpanzees attempted to use social cues to locate hidden food in one of two possible hiding places. In the first study four chimpanzees were exposed to a local enhancement cue (the informant approached and looked to the location where food was hidden and then remained beside it) and a gaze/point cue (the informant gazed and manually pointed towards the location where the food was hidden). Each cue was given by both a human informant and a chimpanzee informant. In the second study 12 chimpanzees were exposed to a gaze direction cue in combination with a vocal cue (the human informant gazed to the hiding location and produced one of two different vocalizations: a ‘food-bark’ or a human word-form). The results were: (i) all subjects were quite skillful with the local enhancement cue, no matter who produced it; (ii) few subjects were skillful with the gaze/point cue, no matter who produced it (most of these being individuals who had been raised in infancy by humans); and (iii) most subjects were skillful when the human gazed and vocalized at the hiding place, with little difference between the two types of vocal cue. Findings are discussed in terms of chimpanzees’ apparent need for additional cues, over and above gaze direction cues, to indicate the presence of food.     

Chimpanzees’ (Pan troglodytes) use of gaze cues in object-choice tasks: different methods yield different results

To assess the influence of different procedures on chimpanzees' performance in object-choice tasks, five adult chimpanzees were tested using three experimenter-given cues to food location: gazing, glancing, and pointing. These cues were delivered to the subjects in an identical fashion but were deployed within the context of two distinct meta-procedures that have been previously employed with this species with conflicting results. In one procedure, the subjects entered the test unit and approached the experimenter (who had already established the cue) on each trial. In the other procedure, the subjects stayed in the test unit throughout a session, witnessed the hiding procedure, and waited for a delay of 10 s during which the cue was provided. The subjects scored at high levels far exceeding chance in response to the gaze cue only when they approached the experimenter for each trial. They performed at chance levels when they stayed inside the test unit throughout the session. They scored at chance levels on all other cues irrespective of the procedure. These findings imply that (a) chimpanzees can immediately exploit social gaze cues, and (b) previous conflicting findings were likely due to the different meta-procedures that were used.     

自闭症儿童利用社会性注意线索习得词语的眼动研究

本研究采用眼动技术考察18名自闭症儿童利用社会性注意线索习得词语的能力。结果表明：1）自闭症儿童具有利用他人视线习得词语的能力;2）不同视线对自闭症儿童的词语习得产生不同的影响;3）自闭症儿童视线追随行为的潜在机制与普通儿童存在差异,自闭症儿童的视线追随行为可能是意识性的诱发行为而普通儿童则是反射性的自发行为。     

Gaze discrimination learning in olive baboons (Papio anubis)

The ability to discriminate between pairs of photographs according to the portrayed model's visual attention status was examined in four olive baboons. Two baboons successfully managed to solve the problem, even when attention was demonstrated by eye direction alone. A third showed an ability to discriminate head direction but not eye direction. In order to investigate further their ability to discriminate attention, the two successful baboons and two na?ve baboons were presented with a simple object-choice task accompanied by experimenter-given cues. There was no evidence of transfer from the photographic stimuli to a real model; only one baboon showed signs of using the experimenter's attention to chose between two objects, and only after over 300 trials. These results could suggest that the baboons used simple physical cues rather than a concept of attention to solve the picture discrimination but alternative explanations are also discussed. Accepted after revision: 5 February 2001 Electronic Publication     

Gaze,goals and growing up: Effects on imitative grasping

Developmental differences in the use of social‐attention cues to imitation were examined among children aged 3 and 6 years old (n = 58) and adults (n = 29). In each of 20 trials, participants watched a model grasp two objects simultaneously and move them together. On every trial, the model directed her gaze towards only one of the objects. Some object pairs were related and had a clear functional relationship (e.g., flower, vase), while others were functionally unrelated (e.g., cardboard square, ladybug). Owing to attentional effects of eye gaze, it was expected that all participants would more faithfully imitate the grasp on the gazed‐at object than the object not gazed‐at. Children were expected to imitate less faithfully on trials with functionally related objects than those without, due to goal‐hierarchy effects. Results support effects of eye gaze on imitation of grasping. Children's grasping accuracy on functionally related and functionally unrelated trials was similar, but they were more likely to only use one hand on trials where the object pairs were functionally related than unrelated. Implications for theories of imitation are discussed.     

Use of human visual attention cues by olive baboons (Papio anubis) in a competitive task

The ability of 4 olive baboons (Papio anubis) to use human gaze cues during a competitive food task was investigated. Three baboons used head orientation as a cue, and 1 individual also used eye direction alone. As the baboons did not receive prior training with gestural cues, their performance suggests that the competitive paradigm may be more appropriate for testing nonhuman primates than the standard object-choice paradigm. However, the baboons were insensitive to whether the experimenter could actually perceive the food item, and therefore the use of visual orientation cues may not be indicative of visual perspective-taking abilities. Performance was disrupted by the introduction of a screen and objects to conceal food items and by the absence of movement in cues presented.     

Can dogs use vocal intonation as a social referencing cue in an object choice task?

Evidence from the literature indicates that dogs’ choices can be influenced by human-delivered social cues, such as pointing, and pointing combined with facial expression, intonation (i.e., rising and falling voice pitch), and/or words. The present study used an object choice task to investigate whether intonation conveys unique information in the absence of other salient cues. We removed facial expression cues and speech information by delivering cues with the experimenter’s back to the dog and by using nonword vocalizations. During each trial, the dog was presented with pairs of the following three vocal cues: Positive (happy-sounding), Negative (sad-sounding), and Breath (neutral control). In Experiment 1, where dogs received only these vocal cue pairings, dogs preferred the Positive intonation, and there was no difference in choice behavior between Negative or Breath. In Experiment 2, we included a point cue with one of the two vocal cues in each pairing. Here, dogs preferred containers receiving pointing cues as well as Negative intonation, and preference was greatest when both of these cues were presented together. Taken together, these findings indicate that dogs can indeed extract information from vocal intonation alone, and may use intonation as a social referencing cue. However, the effect of intonation on behavior appears to be strongly influenced by the presence of pointing, which is known to be a highly salient visual cue for dogs. It is possible that in the presence of a point cue, intonation may shift from informative to instructive.     

How monkeys see the eyes: cotton-top tamarins’ reaction to changes in visual attention and action

Among social species, the capacity to detect where another individual is looking is adaptive because gaze direction often predicts what an individual is attending to, and thus what its future actions are likely to be. We used an expectancy violation procedure to determine whether cotton-top tamarins (Saguinus oedipus oedipus) use the direction of another individual’s gaze to predict future actions. Subjects were familiarized with a sequence in which a human actor turned her attention toward one of two objects sitting on a table and then reached for that object. Following familiarization, subjects saw two test events. In one test event, the actor gazed at the new object and then reached for that object. From a human perspective, this event is considered consistent with the causal relationship between visual attention and subsequent action, that is, grabbing the object attended to. In the second test event, the actor gazed at the old object, but reached for the new object. This event is considered a violation of expectation. When the actor oriented with both her head-and-eyes, subjects looked significantly longer at the second test event in which the actor reached for the object to which she had not previously oriented. However, there was no difference in looking time between test events when the actor used only her eyes to orient. These findings suggest that tamarins are able to use some combination of head orientation and gaze direction, but not gaze direction alone, to predict the actions of a human agent. Received: 17 February 1999 / Accepted after revision: 9 May 1999