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.     

Gorillas’ (Gorilla gorilla) use of experimenter-given manual and facial cues in an object-choice task

Several experiments have been performed to examine the great apes’ use of experimenter-given manual and visual cues in object-choice tasks. Considering their use of referential gestures in gaze-following paradigms, great apes perform surprisingly unsuccessfully in object-choice tasks. However, the large majority of object-choice experiments have been conducted with chimpanzees (Pan troglodytes) with very few experiments including other great ape species, making it difficult to generalize about the great apes. Interestingly, the only object-choice task conducted with gorillas (Gorilla gorilla) has indicated successful use of both manual and visual cues. It was the aim of the present study to gather more data on gorillas’ use of human manual and facial cues on the object-choice task. Gorilla subjects in this study did not show consistent use of three types of referential cues.     

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     

Use of experimenter-given cues in dogs

Since the observations of O. Pfungst the use of human-provided cues by animals has been well-known in the behavioural sciences (“Clever Hans effect”). It has recently been shown that rhesus monkeys (Macaca mulatta) are unable to use the direction of gazing by the experimenter as a cue for finding food, although after some training they learned to respond to pointing by hand. Direction of gaze is used by chimpanzees, however. Dogs (Canis familiaris) are believed to be sensitive to human gestural communication but their ability has never been formally tested. In three experiments we examined whether dogs can respond to cues given by humans. We found that dogs are able to utilize pointing, bowing, nodding, head-turning and glancing gestures of humans as cues for finding hidden food. Dogs were also able to generalize from one person (owner) to another familiar person (experimenter) in using the same gestures as cues. Baseline trials were run to test the possibility that odour cues alone could be responsible for the dogs’ performance. During training individual performance showed limited variability, probably because some dogs already “knew” some of the cues from their earlier experiences with humans. We suggest that the phenomenon of dogs responding to cues given by humans is better analysed as a case of interspecific communication than in terms of discrimination learning. Received: 30 May 1998 / Accepted after revision: 6 September 1998     

The use of experimenter-given cues by South African fur seals (<Emphasis Type="Italic">Arctocephalus pusillus</Emphasis>)

Dogs can use a variety of experimenter-given cues such as pointing, head direction, and eye direction to locate food hidden under one of several containers. Some authors have proposed that this is a result of the domestication process. In this study we tested four captive fur seals in a two alternative object choice task in which subjects had to use one of the following experimenter-given cues to locate the food: (1) the experimenter pointed and gazed at one of the objects, (2) the experimenter pointed at only one of the objects, (3) the experimenter gazed at only one of the objects, (4) the experimenter glanced at only one of the objects, (5) the experimenter pointed and gazed at one of the objects but was sitting closer to one object than to the other, (6) the experimenter pointed only with the index finger at one of the objects, (7) the experimenter presented a replica of one of the objects. The fur seals were able to use cues which involved a fully exposed arm or a head direction, but failed to use glance only, the index finger pointing and the object replica cues. The results showed that a domestication process was not necessary to develop receptive skills to cues given by an experimenter. Instead, we hypothesize that close interactions with humans prior to testing enabled fur seals to use some gestural cues without formal training. We also analyzed the behavior of the seals depending on the level of difficulty of the task. Behavioral signs of hesitation increased with task difficulty. This suggests that the fur seals were sensitive to task difficulty.     

The chimpanzee mind: in search of the evolutionary roots of the human mind

One advantage of living in a social group is the opportunity to use information provided by other individuals. Social information can be based on cues provided by a conspecific or even by a heterospecific individual (e.g., gaze direction, vocalizations, pointing gestures). Although the use of human gaze and gestures has been extensively studied in primates, and is increasingly studied in other mammals, there is no documentation of birds using these cues in a cooperative context. In this study, we tested the ability of three African gray parrots to use different human cues (pointing and/or gazing) in an object-choice task. We found that one subject spontaneously used the most salient pointing gesture (looking and steady pointing with hand at about 20 cm from the baited box). The two others were also able to use this cue after 15 trials. None of the parrots spontaneously used the steady gaze cues (combined head and eye orientation), but one learned to do so effectively after only 15 trials when the distance between the head and the baited box was about 1 m. However, none of the parrots were able to use the momentary pointing nor the distal pointing and gazing cues. These results are discussed in terms of sensitivity to joint attention as a prerequisite to understand pointing gestures as it is to the referential use of labels.     

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.     

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.     

Bottlenosed dolphins (Tursiops truncatus) comprehend the referent of both static and dynamic human gazing and pointing in an object-choice task

The authors tested 2 bottlenosed dolphins (Tursiops truncatus) for their understanding of human-directed gazing or pointing in a 2-alternative object-choice task. A dolphin watched a human informant either gazing at or pointing toward 1 of 2 laterally placed objects and was required to perform a previously indicated action to that object. Both static and dynamic gaze, as well as static and dynamic direct points and cross-body points, yielded errorless or nearly errorless performance. Gaze with the informant's torso obscured (only the head was shown) produced no performance decrement, but gaze with eyes only resulted in chance performance. The results revealed spontaneous understanding of human gaze accomplished through head orientation, with or without the human informant's eyes obscured, and demonstrated that gaze-directed cues were as effective as point-directed cues in the object-choice task.     

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.     

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.     

Comprehension of human communicative signs in pet dogs (Canis familiaris).

On the basis of a study by D. J. Povinelli, D. T. Bierschwale, and C. G. Cech (1999), the performance of family dogs (Canis familiaris) was examined in a 2-way food choice task in which 4 types of directional cues were given by the experimenter: pointing and gazing, head-nodding ("at target"), head turning above the correct container ("above target"), and glancing only ("eyes only"). The results showed that the performance of the dogs resembled more closely that of the children in D. J. Povinelli et al.'s study, in contrast to the chimpanzees' performance in the same study. It seems that dogs, like children, interpret the test situation as being a form of communication. The hypothesis is that this similarity is attributable to the social experience and acquired social routines in dogs because they spend more time in close contact with humans than apes do, and as a result dogs are probably more experienced in the recognition of human gestures.     

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     

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.     

A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans

Dogs' (Canis familiaris) and cats' (Felis catus) interspecific communicative behavior toward humans was investigated. In Experiment 1, the ability of dogs and cats to use human pointing gestures in an object-choice task was compared using 4 types of pointing cues differing in distance between the signaled object and the end of the fingertip and in visibility duration of the given signal. Using these gestures, both dogs and cats were able to find the hidden food; there was no significant difference in their performance. In Experiment 2, the hidden food was made inaccessible to the subjects to determine whether they could indicate the place of the hidden food to a naive owner. Cats lacked some components of attention-getting behavior compared with dogs. The results suggest that individual familiarization with pointing gestures ensures high-level performance in the presence of such gestures; however, species-specific differences could cause differences in signaling toward the human.     

Preschool children's use of cues to generic meaning

Sentences that refer to categories - generic sentences (e.g., "Dogs are friendly") - are frequent in speech addressed to young children and constitute an important means of knowledge transmission. However, detecting generic meaning may be challenging for young children, since it requires attention to a multitude of morphosyntactic, semantic, and pragmatic cues. The first three experiments tested whether 3- and 4-year-olds use (a) the immediate linguistic context, (b) their previous knowledge, and (c) the social context to determine whether an utterance with ambiguous scope (e.g., "They are afraid of mice", spoken while pointing to 2 birds) is generic. Four-year-olds were able to take advantage of all the cues provided, but 3-year-olds were sensitive only to the first two. In Experiment 4, we tested the relative strength of linguistic-context cues and previous-knowledge cues by putting them in conflict; in this task, 4-year-olds, but not 3-year-olds, preferred to base their interpretations on the explicit noun phrase cues from the linguistic context. These studies indicate that, from early on, children can use contextual and semantic information to construe sentences as generic, thus taking advantage of the category knowledge conveyed in these sentences.     

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.     

On the relationship between categorical frequency estimation and cued recall

In a categorical frequency-estimation task, subjects have to indicate the number of exemplars from particular categories that have been shown on a list. In three experiments, the relationship between this task and the recall of exemplars with category names as cues was investigated. Three variables (generation, blocking of category exemplars, and provision of extralist cues) were shown to have identical effects on the two tasks. These results support a model of categorical frequency estimation in which subjects use a category name to retrieve exemplars and then base their frequency estimate on a count of the exemplars that have been retrieved.     

Temporal parameters as cues to phrasal boundaries: a comparison of processing by left- and right-hemisphere brain-damaged individuals

Two experiments were conducted to examine the ability of left- (LHD) and right-hemisphere-damaged (RHD) patients and normal controls to use temporal cues in rendering phrase grouping decisions. The phrase "pink and black and green" was manipulated to signal a boundary after "pink" or after "black" by altering pre-boundary word durations and pause durations at the boundary in a stepwise fashion. Stimuli were presented to listeners auditorily along with a card with three alternative groupings of colored squares from which to select the presented alternative. Results revealed that normal controls were able to use both temporal cues to identify the intended grouping. In contrast, LHD patients required longer than normal pause durations to consistently identify the intended grouping, suggesting a higher than normal threshold for perception of temporal prosodic cues. Surprisingly, the RHD patients exhibited great difficulty with the task, perhaps due to the limited acoustic cues available in the stimuli.     

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.