Ádám Miklósi

Use of experimenter-given cues in dogs

Abstract 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.

A comparative analysis of animals' understanding of the human pointing gesture

We review studies demonstrating the ability of some animals to understand the human pointing gesture. We present a 3-step analysis of the topic. (1) We compare and evaluate current experimental methods (2) We compare available experimental results on performance of different species and investigate the interaction of species differences and other independent variables (3) We evaluate how our present understanding of pointing comprehension answers questions about function, evolution and mechanisms. Recently, a number of different hypotheses have been put forward to account for the presence of this ability in some species and for the lack of such comprehension in others. In our view, there is no convincing evidence for the assumption that the competitive lifestyles of apes would inhibit the utilization of this human gesture. Similarly, domestication as a special evolutionary factor in the case of some species falls short in explaining high levels of pointing comprehension in some non-domestic species. We also disagree with the simplistic view of describing the phenomenon as a simple form of conditioning. We suggest that a more systematic comparative research is needed to understand the emerging communicative representational abilities in animals that provide the background for comprehending the human pointing gesture.

Intentional behaviour in dog-human communication: an experimental analysis of “showing” behaviour in the dog

Abstract Despite earlier scepticism there is now evidence for simple forms of intentional and functionally referential communication in many animal species. Here we investigate whether dogs engage in functional referential communication with their owners. “Showing” is defined as a communicative action consisting of both a directional component related to an external target and an attention-getting component that directs the attention of the perceiver to the informer or sender. In our experimental situation dogs witness the hiding of a piece of food (or a favourite toy) which they cannot get access to. We asked whether dogs would engage in “showing” in the presence of their owner. To control for the motivational effects of both the owner and the food on the dogs’ behaviour, control observations were also staged where only the food (or the toy) or the owner was present. Dogs’ gazing frequency at both the food (toy) and the owner was greater when only one of these was present. In other words, dogs looked more frequently at their owner when the food (toy) was present, and they looked more at the location of the food (toy) when the owner was present. When both the food (toy) and the owner were present a new behaviour, “gaze alternation”, emerged which was defined as changing the direction of the gaze from the location of the food (toy) to looking at the owner (or vice versa) within 2 s. Vocalisations that occurred in this phase were always associated with gazing at the owner or the location of the food. This behaviour, which was specific to this situation, has also been described in chimpanzees, a gorilla and humans, and has often been interpreted as a form of functionally referential communication. Based on our observations we argue that dogs might be able to engage in functionally referential communication with their owner, and their behaviour could be described as a form of “showing”. The contribution of domestication and individual learning to the well-developed communicative skills in dogs is discussed and will be the subject of further studies.

Comparative social cognition: What can dogs teach us?

Research in comparative social cognition addresses how challenges of social living have formed the cognitive structures that control behaviours involved in communication, social learning and social understanding. In contrast to the traditional psychological approach, recent investigations take both evolutionary and functional questions into account, but the main emphasis is still on the mechanisms of behaviour. Although in traditional research ‘comparative’ meant mainly comparisons between humans and other primates, ethological influences have led to a broadening of the spectrum of species under study. In this review, we evaluated how the study of dogs broadens our understanding of comparative social cognition. In the early days of ethology, dogs enjoyed considerable interest from ethologists, but during the last 20 years, dogs have rarely been studied by ethological methods. Through a complex evolutionary process, dogs became adapted for living in human society; therefore, the human environment and social setting now represents a natural ecological niche for this species. We have evidence that dogs have been selected for adaptations to human social life, and that these adaptations have led to marked changes in their communicative, social, cooperative and attachment behaviours towards humans. Until now, the study of dogs was hindered by the view that they represent an ‘artificial’ species, but by accepting that dogs are adapted to their niche, as are other ‘natural’ species, comparative investigations can be put into new light.

Dogs' (Canis familiaris) responsiveness to human pointing gestures

In a series of 3 experiments, dogs (Canis familiaris) were presented with variations of the human pointing gesture: gestures with reversed direction of movement, cross-pointing, and different arm extensions. Dogs performed at above chance level if they could see the hand (and index finger) protruding from the human body contour. If these minimum requirements were not accessible, dogs still could rely on the body position of the signaler. The direction of movement of the pointing arm did not influence the performance. In summary, these observations suggest that dogs are able to rely on relatively novel gestural forms of the human communicative pointing gesture and that they are able to comprehend to some extent the referential nature of human pointing.

Human Analogue Safe Haven Effect of the Owner: Behavioural and Heart Rate Response to Stressful Social Stimuli in Dogs

The secure base and safe haven effects of the attachment figure are central features of the human attachment theory. Recently, conclusive evidence for human analogue attachment behaviours in dogs has been provided, however, the owner’s security-providing role in danger has not been directly supported. We investigated the relationship between the behavioural and cardiac response in dogs (N = 30) while being approached by a threatening stranger in separation vs. in the presence of the owner, presented in a balanced order. Non-invasive telemetric measures of heart rate (HR) and heart rate variability (HRV) data during the threatening approaches was compared to periods before and after the encounters. Dogs that showed distress vocalisation during separation (N = 18) and that growled or barked at the stranger during the threatening approach (N = 17) were defined as behaviourally reactive in the given situation. While characteristic stress vocalisations were emitted during separations, the absence of the owner did not have an effect on dogs’ mean HR, but significantly increased the HRV. The threatening approach increased dogs’ mean HR, with a parallel decrease in the HRV, particularly in dogs that were behaviourally reactive to the encounter. Importantly, the HR increase was significantly less pronounced when dogs faced the stranger in the presence of the owner. Moreover, the test order, whether the dog encountered the stranger first with or without its owner, also proved important: HR increase associated with the encounter in separation seemed to be attenuated in dogs that faced the stranger first in the presence of their owner. We provided evidence for human analogue safe haven effect of the owner in a potentially dangerous situation. Similarly to parents of infants, owners can provide a buffer against stress in dogs, which can even reduce the effect of a subsequent encounter with the same threatening stimuli later when the owner is not present.

Are readers of our face readers of our minds? Dogs (Canis familiaris) show situation-dependent recognition of human's attention.

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

Differential sensitivity to human communication in dogs, wolves and human infants

Boxing Clever? Piaget showed that 10-month-old infants will persist in looking for a toy in box A, where it has been placed several times, even after having been shown that it has been moved to box B, whereas 12-month-old infants do not. This phenomenon marks a developmental milestone in human infant cognition that Topál et al. (p. 1269; see the Perspective by Tomasello and Kaminski and the news story by Pennisi) explored in a remarkable series of comparative tests. The results support the view that infants and adult dogs will both persevere in searching erroneously in box A because they regard the placement of the toy by a human experimenter as a social teaching event. By contrast, wolves rapidly learn correctly to search box B. They also observed that infants are able to generalize and thus still persevere when one experimenter places the toy in box A and a second then places the toy in box B. Dogs, however, display episodic learning, and a second experimenter reduces their searching choice to chance. Social interactions with humans govern the way dogs and children learn, but wolves learn by focusing on objects. Ten-month-old infants persistently search for a hidden object at its initial hiding place even after observing it being hidden at another location. Recent evidence suggests that communicative cues from the experimenter contribute to the emergence of this perseverative search error. We replicated these results with dogs (Canis familiaris), who also commit more search errors in ostensive-communicative (in 75% of the total trials) than in noncommunicative (39%) or nonsocial (17%) hiding contexts. However, comparative investigations suggest that communicative signals serve different functions for dogs and infants, whereas human-reared wolves (Canis lupus) do not show doglike context-dependent differences of search errors. We propose that shared sensitivity to human communicative signals stems from convergent social evolution of the Homo and the Canis genera.

Attachment to humans: A comparative study on hand-reared wolves and differently socialized dog puppies

Using the Strange Situation Test originally developed for testing the mother-infant relationship in humans, we compared the attachment behaviour of extensively socialized (hand-reared) dog, Canis familiaris, and wolf, Canis lupus, puppies towards their human caregiver with that of pet dog puppies of the same age. The experiment was designed to study whether (1) dog puppies as young as 16 weeks show attachment to a human caregiver, (2) extensive socialization by human caregivers affects attachment behaviour of dog puppies and (3) evolutionary changes (in the form of species-specific differences between wolf and dog pups) affect the emergence of dog-human attachment. We found a characteristic selective responsiveness to the owner in young dogs, similar to that observed in adults. This finding supports the view that puppies show patterns of attachment towards their owners. Extensive socialization had only a minor effect on the attachment behaviour in dog puppies, as the behaviour of pet dogs and hand-reared dogs was basically similar. However, we found a significant species-specific difference between wolves and dogs: both extensively socialized and pet dog puppies were more responsive to the owner than to an unfamiliar human participant, whereas extensively socialized wolves were not. Behavioural differences could be best explained by assuming that selective processes took place in the course of domestication (genetic changes) that are related to the attachment system of the dog.

fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses.

Asymmetries in CNS neuroanatomy are assumed to underlie the widespread cognitive and behavioral asymmetries in vertebrates. Studies in humans have shown that the laterality of some cognitive asymmetries is independent of the laterality of the viscera; discrete mechanisms may therefore regulate visceral and neural lateralization. However, through analysis of visceral, neuroanatomical, and behavioral asymmetries in the frequent-situs-inversus (fsi) line of zebrafish, we show that the principal left-right body asymmetries are coupled to certain brain asymmetries and lateralized behaviors. fsi fish with asymmetry defects show concordant reversal of heart, gut, and neuroanatomical asymmetries in the diencephalon. Moreover, the neuroanatomical reversals in reversed fsi fish correlate with reversal of some behavioral responses in both fry and adult fsi fish. Surprisingly, two behavioral asymmetries do not reverse, suggesting that at least two separable mechanisms must influence functional lateralization in the CNS. Partial reversal of CNS asymmetries may generate new behavioral phenotypes; supporting this idea, reversed fsi fry differ markedly from their normally lateralized siblings in their behavioral response to a novel visual feature. Revealing a link between visceral and brain asymmetry and lateralized behavior, our studies help to explain the complexity of the relationship between the lateralities of visceral and neural asymmetries.