Attributing attention: the use of human-given cues by domestic horses (Equus caballus)

Recent research has shown that domestic dogs are particularly good at determining the focus of human attention, often outperforming chimpanzees and hand-reared wolves. It has been suggested that the close evolutionary relationship between humans and dogs has led to the development of this ability; however, very few other domestic species have been studied. We tested the ability of 36 domestic horses to discriminate between an attentive and inattentive person in determining whom to approach for food. The cues provided were body orientation, head orientation or whether the experimenters’ eyes were open or closed. A fourth, mixed condition was included where the attentive person stood with their body facing away from the subjects but their head turned towards the subject while the inattentive person stood with their body facing the subject but their head turned away. Horses chose the attentive person significantly more often using the body cue, head cue, and eye cue but not the mixed cue. This result suggests that domestic horses are highly sensitive to human attentional cues, including gaze. The possible role of evolutionary and environmental factors in the development of this ability is discussed.     

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.     

Attention to attention in domestic dog (Canis familiaris) dyadic play

The social cognitive capacities of dogs, including their communication skills and use of visual attention cues, have recently been investigated in numerous experimental studies. This paper reports on research of domestic dog behavior in a natural setting, which shows sensitivity to the visual attention of their partners when engaged in dyadic rough-and-tumble play. The sequential behaviors and head-direction of both dogs were noted throughout the bouts. The behaviors were differentially used according to the partner’s posture. Play signals were sent nearly exclusively to forward-facing conspecifics; attention-getting behaviors were used most often when a playmate was facing away, and before signaling an interest to play. In addition, the mode of attention-getter matched the degree of inattentiveness of the playmate: stronger attention-getters were used when a playmate was looking away or distracted, less forceful ones when the partner was facing forward or laterally. In other words, these dogs showed attention to, and acted to manipulate, a feature of other dogs that mediates their ability to respond: which feature in human interaction is called “attention”.

Socially dependent auditory laterality in domestic horses (Equus caballus)

Laterality is now known to be an ubiquitous phenomenon among the vertebrates. Particularly, laterality of auditory processing has been demonstrated in a variety of species, especially songbirds and primates. Such a hemispheric specialization has been shown to depend on factors such as sound structure, species specificity and types of stimuli. Much less is known on the possible influence of social familiarity although a few studies suggest such an influence. Here we tested the influence of the degree of familiarity on the laterality of the auditory response in the domestic horse. This species is known for its social system and shows visible reactions to sounds, with one or two ears moving towards a sound source. By comparing such responses to the playback of different conspecific whinnies (group member, neighbor and stranger), we could demonstrate a clear left hemisphere (LH) preference for familiar neighbor calls while no preference was found for group member and stranger calls. Yet, we found an opposite pattern of ear side preference for neighbor versus stranger calls. These results are, to our knowledge, the first to demonstrate auditory laterality in an ungulate species. They open further lines of thought on the influence of the social “value” of calls and the listener’s arousal on auditory processing and laterality.     

Lateralized suckling in domestic horses (Equus caballus)

Brain lateralization enables preferential processing of certain stimuli and more effective utilization of these stimuli in either the left or the right cerebral hemisphere. Horses show both motor and sensory lateralization patterns. Our aim was to determine whether a lateralized response could be detected in foals during the naturally side-biased behaviour, suckling. The foals’ preferred suckling side could be the effect of either visual or motor lateralization. In the case of a visual lateralized response, foals are expected to suck more often from the mother’s right side, so potential danger can be detected by the better adapted right hemisphere (i.e. left eye). Motor lateralization can be identified when a foal will suck predominantly from one side, either left or right. We found no population trend in the preferred suckling side, but we detected significant differences amongst individual foals. One-third (35.4 %) of 79 foals showed a strong, either right or left side preference which increased with age. The mothers did not influence the foals’ suckling side preferences either by side-biased rejection or termination of suckling. According to our findings, a general pattern of sucking with the left eye open for better danger detection and recognition is unlikely in foals up to 7 months old. Foals of this age are probably young or fully focused on suckling and rely on their mothers’ vigilance. Individual side preferences amongst foals are suggested to be based on motor lateralization.     

Domestic dogs (Canis familiaris) use a physical marker to locate hidden food

Dogs can use the placement of an arbitrary marker to locate hidden food in an object-choice situation. We tested domestic dogs (Canis familiaris) in three studies aimed at pinning down the relative contributions of the human’s hand and the marker itself. We baited one of two cups (outside of the dogs’ view) and gave the dog a communicative cue to find the food. Study 1 systematically varied dogs’ perceptual access to the marker placing event, so that dogs saw either the whole human, the hand only, the marker only, or nothing. Follow-up trials investigated the effect of removing the marker before the dog’s choice. Dogs used the marker as a communicative cue even when it had been removed prior to the dog’s choice and attached more importance to this cue than to the hand that placed it although the presence of the hand boosted performance when it appeared together with the marker. Study 2 directly contrasted the importance of the hand and the marker and revealed that the effect of the marker diminished if it had been associated with both cups. In contrast touching both cups with the hand had no effect on performance. Study 3 investigated whether the means of marker placement (intentional or accidental) had an effect on dogs’ choices. Results showed that dogs did not differentiate intentional and accidental placing of the marker. These results suggest that dogs use the marker as a genuine communicative cue quite independently from the experimenter’s actions.     

Neophilia in domestic dogs (Canis familiaris) and its implication for studies of dog cognition

This study examined novel-object preference in dogs. In a free choice test 17 dogs were presented with a novel toy in a line up with two familiar toys. The unfamiliar object was chosen first in 38 out 50 tests suggesting a strong preference for novel over familiar items. Neophilia may be an adaptive trait for domestic dogs that has helped their adaptation towards man.     

Long-term memory for categories and concepts in horses (Equus caballus)

Three horses (Equus caballus) with a history of performing cognitive tasks including discrimination learning, categorization, and concept use were tested to evaluate their long-term memory (LTM) in three experiments. In addition, use of LCD multi-displays for stimulus presentation was incorporated into cognition testing protocol for the first time with horses. Experiment 1 tested LTM for discrimination learning that originally occurred 6 years earlier. Five sets of stimuli were used and the two horses tested showed no decrement in performance on four of the sets; however, both horses did score below chance on one set. Experiment 2 examined long-term categorization recall 10 years after horses had demonstrated the ability to make stimulus selections based on shared characteristics within a given category. The horse tested for LTM after the decade-long interval immediately and consistently applied the previously learned categorization rule to not only familiar but also novel sets of stimuli. Experiment 3 tested another horse for LTM for a relative size concept. This horse had originally demonstrated concept rule use in order to select stimuli based on their relative size to one another. More than 7 years later and without further training, this horse reliably applied the previously established size concept to both familiar and novel sets of stimuli. These findings are the first reports of long-term categorical and conceptual memory in horses and are consistent with observations of domestic and wild horses, which indicate that behavioral and ecological events may be remembered for long periods of time. These studies also demonstrate the adaptive nature of horses with regard to their ability to generalize over several different testing conditions.     

Effect of training and familiarity on responsiveness to human cues in domestic dogs (Canis familiaris)

Domestic dogs (Canis familiaris) seem to possess an evolved competency to follow human-given cues, often out-performing their wild progenitor the wolf (Canis lupus) on cue-following tasks. However, domestication may not be solely responsible for the socio-cognitive skills of dogs, with ontogenetic experience also playing a role. This research evaluated the effects of intensive training on cue-following behaviour using an unreinforced object-choice paradigm. The responses of dogs that were trained to competitive levels were compared to those of pet dogs with only basic training, and dogs living in an animal shelter that demonstrated no or only rudimentary following of basic commands. Using a cue-following task where three types of cues were presented by familiar and unfamiliar human partners, the number of cues followed by each training group were recorded. All dogs found cues where gesture was combined with a congruent head and eye movement easier to follow than either gesture or eye gaze alone. Whether the cue-giver was familiar or not had a significant effect on number of cues followed in homed dogs, and the performance of shelter dogs was comparable to the other groups when faced with an unfamiliar cue-giver. Contrary to predictions, level of training did not improve performance on the cue-following task. This work does provide support for the presence of an evolved adaptation to exploit social cues provided by humans that can be augmented by familiarity with the cue giver. However, additional joint activity as experienced in an intensive training regime does not seem to increase accuracy in following human-given cues.     

Cross-modal recognition of human individuals in domestic horses (Equus caballus)

This study has shown that domestic horses are capable of cross-modal recognition of familiar humans. It was demonstrated that horses are able to discriminate between the voices of a familiar and an unfamiliar human without seeing or smelling them at the same moment. Conversely, they were able to discriminate the same persons when only exposed to their visual and olfactory cues, without being stimulated by their voices. A cross-modal expectancy violation setup was employed; subjects were exposed both to trials with incongruent auditory and visual/olfactory identity cues and trials with congruent cues. It was found that subjects responded more quickly, longer and more often in incongruent trials, exhibiting heightened interest in unmatched cues of identity. This suggests that the equine brain is able to integrate multisensory identity cues from a familiar human into a person representation that allows the brain, when deprived of one or two senses, to maintain recognition of this person.     

Cues to food location that domestic dogs (Canis familiaris) of different ages do and do not use

The results of three experiments are reported. In the main study, a human experimenter presented domestic dogs (Canis familiaris) with a variety of social cues intended to indicate the location of hidden food. The novel findings of this study were: (1) dogs were able to use successfully several totally novel cues in which they watched a human place a marker in front of the target location; (2) dogs were unable to use the marker by itself with no behavioral cues (suggesting that some form of human behavior directed to the target location was a necessary part of the cue); and (3) there were no significant developments in dogs’ skills in these tasks across the age range 4 months to 4 years (arguing against the necessity of extensive learning experiences with humans). In a follow-up study, dogs did not follow human gaze into “empty space” outside of the simulated foraging context. Finally, in a small pilot study, two arctic wolves (Canis lupus) were unable to use human cues to locate hidden food. These results suggest the possibility that domestic dogs have evolved an adaptive specialization for using human-produced directional cues in a goal-directed (especially foraging) context. Exactly how they understand these cues is still an open question. Received: 28 April 2000 / Accepted after revision: 2 September 2000     

Hierarchical stimulus processing by dogs (Canis familiaris)

The purpose of this study was to assess the visual processing of global and local levels of hierarchical stimuli in domestic dogs. Fourteen dogs were trained to recognise a compound stimulus in a simultaneous conditioned discrimination procedure and were then tested for their local/global preference in a discrimination test. As a group, dogs showed a non-significant trend for global precedence, although large inter-individual variability was observed. Choices in the test were not affected by either dogs’ sex or the type of stimulus used for training. However, the less time a dog took to complete the discrimination training phase, the higher the probability that it chose the global level of test stimulus. Moreover, dogs that showed a clear preference for the global level in the test were significantly less likely to show positional responses during discrimination training. These differences in the speed of acquisition and response patterns may reflect individual differences in the cognitive requirements during discrimination training. The individual variability in global/local precedence suggests that experience in using visual information may be more important than predisposition in determining global/local processing in dogs.     

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     

An investigation on the olfactory capabilities of domestic dogs (Canis lupus familiaris)

Animal Cognition - The extraordinary olfactory capabilities in detection and rescue dogs are well-known. However, the olfactory performance varies by breed and search environment (Jezierski...     

Discrimination of human and dog faces and inversion responses in domestic dogs (Canis familiaris)

Although domestic dogs can respond to many facial cues displayed by other dogs and humans, it remains unclear whether they can differentiate individual dogs or humans based on facial cues alone and, if so, whether they would demonstrate the face inversion effect, a behavioural hallmark commonly used in primates to differentiate face processing from object processing. In this study, we first established the applicability of the visual paired comparison (VPC or preferential looking) procedure for dogs using a simple object discrimination task with 2D pictures. The animals demonstrated a clear looking preference for novel objects when simultaneously presented with prior-exposed familiar objects. We then adopted this VPC procedure to assess their face discrimination and inversion responses. Dogs showed a deviation from random behaviour, indicating discrimination capability when inspecting upright dog faces, human faces and object images; but the pattern of viewing preference was dependent upon image category. They directed longer viewing time at novel (vs. familiar) human faces and objects, but not at dog faces, instead, a longer viewing time at familiar (vs. novel) dog faces was observed. No significant looking preference was detected for inverted images regardless of image category. Our results indicate that domestic dogs can use facial cues alone to differentiate individual dogs and humans and that they exhibit a non-specific inversion response. In addition, the discrimination response by dogs of human and dog faces appears to differ with the type of face involved.     

The effect of repeated testing on judgement bias in domestic dogs (Canis familiaris)

Animal Cognition - Judgement bias paradigms are increasingly being used as a measure of affective state in dogs. Approach to an ambiguous stimulus is commonly used as a measure of affect, however,...     

Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study

Empathy covers a range of phenomena from cognitive empathy involving metarepresentation to emotional contagion stemming from automatically triggered reflexes. An experimental protocol first used with human infants was adapted to investigate empathy in domestic dogs. Dogs oriented toward their owner or a stranger more often when the person was pretending to cry than when they were talking or humming. Observers, unaware of experimental hypotheses and the condition under which dogs were responding, more often categorized dogs' approaches as submissive as opposed to alert, playful or calm during the crying condition. When the stranger pretended to cry, rather than approaching their usual source of comfort, their owner, dogs sniffed, nuzzled and licked the stranger instead. The dogs' pattern of response was behaviorally consistent with an expression of empathic concern, but is most parsimoniously interpreted as emotional contagion coupled with a previous learning history in which they have been rewarded for approaching distressed human companions.     

Visual discrimination of species in dogs (Canis familiaris)

In most social interactions, an animal has to determine whether the other animal belongs to its own species. This perception may be visual and may involve several cognitive processes such as discrimination and categorization. Perceptual categorization is likely to be involved in species characterized by a great phenotypic diversity. As a consequence of intensive artificial selection, domestic dogs, Canis familiaris, present the largest phenotypic diversity among domestic mammals. The goal of our study was to determine whether dogs can discriminate any type of dog from other species and can group all dogs whatever their phenotypes within the same category. Nine pet dogs were successfully trained through instrumental conditioning using a clicker and food rewards to choose a rewarded image, S+, out of two images displayed on computer screens. The generalization step consisted in the presentation of a large sample of paired images of heads of dogs from different breeds and cross-breeds with those of other mammal species, included humans. A reversal phase followed the generalization step. Each of the nine subjects was able to group all the images of dogs within the same category. Thus, the dogs have the capacity of species discrimination despite their great phenotypic variability, based only on visual images of heads.     

Spatial memory of domestic dogs (Canis familiaris) for hidden objects in a detour task

Spatial memory of domestic dogs (Canis familiaris) for hidden objects was investigated via a visible displacement problem of object permanence with a detour paradigm. Experiment 1 showed that dogs were able to spontaneously locate a disappearing object in a detour situation. In Experiments 2 and 3, dead reckoning and allocentric spatial information were put in conflict. Results revealed that dogs simultaneously encoded both sources of information when they had to bypass an obstacle to locate a hidden object. Experiment 3 also revealed that, over the course of testing, dogs gradually learned to rely predominantly on allocentric cues when the detour involved several reorientations. The current study reveals that spatial memory of dogs for hidden objects in a detour task was guided by flexibility in processing spatial information. Dogs could simultaneously encode dead reckoning and allocentric information to locate a disappearing object and used them hierarchically according to the complexity of the detour they encountered in the environment.     

Waiting for more: the performance of domestic dogs (Canis familiaris) on exchange tasks

Five domestic dogs (Canis familiaris) were tested in a cooperative exchange task with an experimenter, as previously tested in non-human primates. In the first task, the dogs exchanged to maximise payoffs when presented with food items of differing quality. All consistently exchanged lower-value for higher-value rewards, as determined by their individual food preference, and exchanges corresponded significantly with the spontaneous preferences of three dogs. Next, all subjects demonstrated an ability to perform two and three exchanges in succession, to gain both qualitative and quantitatively increased rewards (group mean = 72 and 92% successful triple exchanges, respectively). Finally, the ability to delay gratification over increasing intervals was tested; the dogs kept one food item to exchange later for a larger item. As previously reported in non-human primates, there was considerable individual variation in the tolerance of delays, between 10 s and 10 min for the largest rewards. For those who reached longer time lags (>40 s), the dogs gave up the chance to exchange earlier than expected by each subject’s general waiting capacity; the dogs anticipated delay duration and made decisions according to the relative reward values offered. Compared to primates, dogs tolerated relatively long delays for smaller value rewards, suggesting that the socio-ecological history of domestic dogs facilitates their performance on decision-making and delay of gratification tasks.