The effect of oxytocin on human-directed social behaviour in dogs (Canis familiaris)

The oxytocin system has recently received increasing attention due to its effect on complex human behaviours. In parallel to this, over the past couple of decades, the human-analogue social behaviour of dogs has been intensively studied. Combining these two lines of research (e.g. studying the relationship between dog social behaviour and the oxytocin system) is a promising new research area. The present paper reviews the existing literature on how oxytocin is related to different aspects of human-directed social behaviour in dogs.     

Separation Anxiety,Attachment and Inter-Personal Representations: Disentangling the Role of Oxytocin in the Perinatal Period

In this paper, we aimed to assess cross-sectionally and longitudinally associations between disturbances in maternal early attachment experiences, symptoms of separation anxiety and depression and oxytocin plasma levels. We examined a mediational model that tested the hypothesis that anxious attachment style arising from the mothers’ early bonding experiences with her own parents was associated with high levels of separation anxiety which, via its impact on depression, was associated with reduced levels of oxytocin in the postnatal period. Data is reported on a structured sample of 127 women recruited during pregnancy from a general hospital antenatal clinic and an initial follow up cohort of 57 women who were re-assessed at 3-months post-partum. We found an association between lower oxytocin level in the post partum period and symptoms of separation anxiety and depression during pregnancy, as well as maternal negative interpersonal representations, upbringing attributes and anxious attachment style. Further meditational analysis revealed that the unique association between anxious attachment and depression is mediated by separation anxiety and that depressed mood mediated the relationship between separation anxiety and oxytocin. In conjunction with evidence from the literature suggesting that lower oxytocin level is associated with bonding difficulties, our findings have significant implications for understanding the biological processes underpinning adverse attachment experiences, negative affect state, and mother-to-infant bonding difficulties.     

Intranasal oxytocin and a polymorphism in the oxytocin receptor gene are associated with human-directed social behavior in golden retriever dogs

The oxytocin system may play an important role in dog domestication from the wolf. Dogs have evolved unique human analogue social skills enabling them to communicate and cooperate efficiently with people. Genomic differences in the region surrounding the oxytocin receptor (OXTR) gene have previously been associated with variation in dogs' communicative skills. Here we have utilized the unsolvable problem paradigm to investigate the effects of oxytocin and OXTR polymorphisms on human-directed contact seeking behavior in 60 golden retriever dogs. Human-oriented behavior was quantified employing a previously defined unsolvable problem paradigm. Behaviors were tested twice in a repeated, counterbalanced design, where dogs received a nasal dose of either oxytocin or saline 45 min before each test occasion. Buccal DNA was analysed for genotype on three previously identified SNP-markers associated with OXTR. The same polymorphisms were also genotyped in 21 wolf blood samples to explore potential genomic differences between the species. Results showed that oxytocin treatment decreased physical contact seeking with the experimenter and one of the three polymorphisms was associated with degree of physical contact seeking with the owner. Dogs with the AA-genotype at this locus increased owner physical contact seeking in response to oxytocin while the opposite effect was found in GG-genotype individuals. Hence, intranasal oxytocin treatment, an OXTR polymorphism and their interaction are associated with dogs' human-directed social skills, which can explain previously described breed differences in oxytocin response. Genotypic variation at the studied locus was also found in wolves indicating that it was present even at the start of dog domestication.     

CD38 regulates oxytocin secretion and complex social behavior

The peptide hormone oxytocin plays a critical role in regulating affiliative behaviors including mating, pair-bond formation, maternal/parenting behavior, social recognition, separation distress and other aspects of attachment. Jin and colleagues recently reported intriguing findings that CD38, a transmembrane receptor with ADP-ribosyl cyclase activity, plays a critical role in maternal nurturing behavior and social recognition by regulating oxytocin secretion. This research may have implications for understanding disorders marked by deficits in social cognition and social functioning, including autism, social anxiety disorder, borderline personality disorder and schizophrenia.     

Human‐directed social behaviour in dogs shows significant heritability

Through domestication and co‐evolution with humans, dogs have developed abilities to attract human attention, e.g. in a manner of seeking assistance when faced with a problem solving task. The aims of this study were to investigate within breed variation in human‐directed contact seeking in dogs and to estimate its genetic basis. To do this, 498 research beagles, bred and kept under standardized conditions, were tested in an unsolvable problem task. Contact seeking behaviours recorded included both eye contact and physical interactions. Behavioural data was summarized through a principal component analysis, resulting in four components: test interactions, social interactions, eye contact and physical contact. Females scored significantly higher on social interactions and physical contact and age had an effect on eye contact scores. Narrow sense heritabilities (h²) of the two largest components were estimated at 0.32 and 0.23 but were not significant for the last two components. These results show that within the studied dog population, behavioural variation in human‐directed social behaviours was sex dependent and that the utilization of eye contact seeking increased with age and experience. Hence, heritability estimates indicate a significant genetic contribution to the variation found in human‐directed social interactions, suggesting that social skills in dogs have a genetic basis, but can also be shaped and enhanced through individual experiences. This research gives the opportunity to further investigate the genetics behind dogs' social skills, which could also play a significant part into research on human social disorders such as autism.     

Oxytocin Receptor Gene Polymorphisms Are Associated with Human Directed Social Behavior in Dogs (Canis familiaris)

The oxytocin system has a crucial role in human sociality; several results prove that polymorphisms of the oxytocin receptor gene are related to complex social behaviors in humans. Dogs'' parallel evolution with humans and their adaptation to the human environment has made them a useful species to model human social interactions. Previous research indicates that dogs are eligible models for behavioral genetic research, as well. Based on these previous findings, our research investigated associations between human directed social behaviors and two newly described (−212AG, 19131AG) and one known (rs8679684) single nucleotide polymorphisms (SNPs) in the regulatory regions (5′ and 3′ UTR) of the oxytocin receptor gene in German Shepherd (N = 104) and Border Collie (N = 103) dogs. Dogs'' behavior traits have been estimated in a newly developed test series consisting of five episodes: Greeting by a stranger, Separation from the owner, Problem solving, Threatening approach, Hiding of the owner. Buccal samples were collected and DNA was isolated using standard protocols. SNPs in the 3′ and 5′ UTR regions were analyzed by polymerase chain reaction based techniques followed by subsequent electrophoresis analysis. The gene–behavior association analysis suggests that oxytocin receptor gene polymorphisms have an impact in both breeds on (i) proximity seeking towards an unfamiliar person, as well as their owner, and on (ii) how friendly dogs behave towards strangers, although the mediating molecular regulatory mechanisms are yet unknown. Based on these results, we conclude that similarly to humans, the social behavior of dogs towards humans is influenced by the oxytocin system.     

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.     

Pet owner behaviors and attachment to yard versus house dogs

Abstract

The majority of research on the human–nonhuman animal bond has considered its advantages for the human. Research investigating the benefits of the bond for the companion animal has focused primarily on the relationship between owner attachment and the relinquishment or abandonment of pets. Shore, Douglas and Riley (2005) compiled a list of 67 behaviors of pet owners of potential benefit to the dog or cat, categorized the behaviors as Essential, Standard, Enriched, or Luxury Care, and studied the relationship between these behaviors and a measure of attachment. The present study continues the investigation of more routine pet-keeping activities by examining the prevalence of such behaviors among a subset of dog owners who keep their dogs out of doors as compared with those whose dogs live primarily in the house. Participants were 322 largely non-traditional college students at a university in the Midwestern United States. Scores on two attachment measures were significantly higher for owners of house dogs as compared with those of owners of yard dogs. Although the majority of both house and yard dogs received basic care, fewer yard dogs received as high levels of attention to some of their physical and safety needs. The gap between yard and house dogs widened as the category of care moved from Essential to Enriched. Involvement in agility training, being taken to events for pets, and exercising with a member of the family were notable exceptions, in that they occurred in equal proportions for yard and house dogs, and perhaps represent opportunities for yard dogs to be in closer contact with a human caretaker. The results suggest that adoptions of sheltered or rescued dogs to people who plan to keep the pet outside can be made with confidence that the dog will be cared for, but that programs to educate the public on the social needs of dogs and the benefits of keeping dogs indoors might result in increased attention to the needs of the animals, strengthening of the human–nonhuman animal bond, and reduction of relinquishment.     

Dog experts' brains distinguish socially relevant body postures similarly in dogs and humans

We read conspecifics' social cues effortlessly, but little is known about our abilities to understand social gestures of other species. To investigate the neural underpinnings of such skills, we used functional magnetic resonance imaging to study the brain activity of experts and non-experts of dog behavior while they observed humans or dogs either interacting with, or facing away from a conspecific. The posterior superior temporal sulcus (pSTS) of both subject groups dissociated humans facing toward each other from humans facing away, and in dog experts, a distinction also occurred for dogs facing toward vs. away in a bilateral area extending from the pSTS to the inferior temporo-occipital cortex: the dissociation of dog behavior was significantly stronger in expert than control group. Furthermore, the control group had stronger pSTS responses to humans than dogs facing toward a conspecific, whereas in dog experts, the responses were of similar magnitude. These findings suggest that dog experts' brains distinguish socially relevant body postures similarly in dogs and humans.     

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.     

Early Life Experiences and Exercise Associate with Canine Anxieties

Personality and anxiety disorders across species are affected by genetic and environmental factors. Shyness-boldness personality continuum exists across species, including the domestic dog, with a large within- and across-breed variation. Domestic dogs are also diagnosed for several anxiety-related behavioral conditions, such as generalized anxiety disorders, phobias, and separation anxiety. Genetic and environmental factors contributing to personality and anxiety are largely unknown. We collected questionnaire data from a Finnish family dog population (N = 3264) in order to study the associating environmental factors for canine fearfulness, noise sensitivity, and separation anxiety. Early life experiences and exercise were found to associate with anxiety prevalence. We found that fearful dogs had less socialization experiences (p = 0.002) and lower quality of maternal care (p < 0.0001) during puppyhood. Surprisingly, the largest environmental factor associating with noise sensitivity (p < 0.0001) and separation anxiety (p = 0.007) was the amount of daily exercise; dogs with noise sensitivity and separation anxiety had less daily exercise. Our findings suggest that dogs share many of the same environmental factors that contribute to anxiety in other species as well, such as humans and rodents. Our study highlights the importance of early life experiences, especially the quality of maternal care and daily exercise for the welfare and management of the dogs, and reveals important confounding factors to be considered in the genetic characterization of canine anxiety.     

Attachment Anxiety and Avoidance Influence Pet Choice and Pet-directed Behaviors

Attachment theory is a useful lens through which to examine both perceptions and selection of companion animals. Study 1 compared perceptions of dogs and cats, and found that dogs were perceived as having more positive relationship qualities and secure attachment-related characteristics, whereas cats were perceived as having more negative relationship qualities and avoidant attachment-related characteristics. In addition, people perceived relationships with dogs to involve less avoidance and less anxiety relative to relationships with people. In study 2, which built on the findings of study 1, attachment avoidance was negatively associated with wanting to own a pet, whereas attachment anxiety was positive associated with wanting to own a pet. These attachment dimensions were not associated with wanting to own a dog, but lower avoidance and higher anxiety were associated with wanting to own a cat. Study 3 was a longitudinal study of SPCA-type shelter visitors (510 participants, with 169 reporting a recent pet adoption). Lower attachment anxiety predicted recently adopting a dog rather than a cat, though neither anxiety nor avoidance predicted adopting a cat. Individuals who wanted a pet in order to facilitate human relationships were more likely to adopt a dog than a cat. Those high in attachment avoidance reported turning to their pet as a replacement for human companionship, and those high in attachment anxiety reported feeling more concern about their pets requiring more attention. Attachment anxiety and avoidance may influence the decision whether or not to adopt a pet, as well as the motivation underlying the adoption choice. Attachment also may influence the type of pet chosen (i.e., dog versus cat). In addition, attachment may influence the nature of the human–animal relationship, such as the time spent together, and the security felt regarding the relationship.     

Children with Avoidant or Disorganized Attachment Relate Differently to a Dog and to Humans During a Socially Stressful Situation

ABSTRACT

Human attachment representations are shaped in interaction with the primary caregiver and are generally transferred to further bonding/ social partners later in life. According to previous evidence, primary attachment representations acquired with humans do not seem to be transferred to companion animals. This was held as a major factor why such animals would effectively provide social support also to persons with insecure attachment. The aim of this study in 19 male children, 7–11 years of age and with insecure-avoidant or disorganized attachment, was to investigate differences in their social behavior and in physiological responses when socially supported by an unfamiliar therapy dog in a socially stressful situation. The Trier Social Stress Test for Children (TSST-C) was conducted to elicit stress in the children when in the presence of the dog and a female human investigator. We found that boys with disorganized attachment (n=11) communicated more intensely than avoidantly attached boys (n=8) with both the dog and humans present. Boys with a disorganized attachment had more physical contact with the dog during the TSST-C and talked more to the dog during and after the TSST-C than did boys with an insecure-avoidant attachment. While the prevailing wisdom holds that attachment representations acquired with the primary human caregiver would not transfer to companion animals, our data indicate otherwise. At least components of attachment-related interaction styles, such as degree of contact seeking in verbal and tactile interactions are also displayed in interaction with animal partners.     

Promotion of sleep by targeting the orexin system in rats, dogs and humans

Orexins are hypothalamic peptides that play an important role in maintaining wakefulness in mammals. Permanent deficit in orexinergic function is a pathophysiological hallmark of rodent, canine and human narcolepsy. Here we report that in rats, dogs and humans, somnolence is induced by pharmacological blockade of both orexin OX(1) and OX(2) receptors. When administered orally during the active period of the circadian cycle, a dual antagonist increased, in rats, electrophysiological indices of both non-REM and, particularly, REM sleep, in contrast to GABA(A) receptor modulators; in dogs, it caused somnolence and increased surrogate markers of REM sleep; and in humans, it caused subjective and objective electrophysiological signs of sleep. No signs of cataplexy were observed, in contrast to the rodent, dog or human narcolepsy syndromes. These results open new perspectives for investigating the role of endogenous orexins in sleep-wake regulation.     

Oxytocin,testosterone, and human social cognition

I describe an integrative social‐evolutionary model for the adaptive significance of the human oxytocinergic system. The model is based on a role for this hormone in the generation and maintenance of social familiarity and affiliation across five homologous, functionally similar, and sequentially co‐opted contexts: mothers with offspring, female and male mates, kin groups, individuals with reciprocity partners, and individuals within cooperating and competing social groups defined by culture. In each situation, oxytocin motivates, mediates and rewards the cognitive and behavioural processes that underlie the formation and dynamics of a more or less stable social group, and promotes a relationship between two or more individuals. Such relationships may be positive (eliciting neurological reward, reducing anxiety and thus indicating fitness‐enhancing effects), or negative (increasing anxiety and distress, and thus motivating attempts to alleviate a problematic, fitness‐reducing social situation). I also present evidence that testosterone exhibits opposite effects from oxytocin on diverse aspects of cognition and behaviour, most generally by favouring self‐oriented, asocial and antisocial behaviours. I apply this model for effects of oxytocin and testosterone to understanding human psychological disorders centrally involving social behaviour. Reduced oxytocin and higher testosterone levels have been associated with under‐developed social cognition, especially in autism. By contrast, some combination of oxytocin increased above normal levels, and lower testosterone, has been reported in a notable number of studies of schizophrenia, bipolar disorder and depression, and, in some cases, higher oxytocin involves maladaptively ‘hyper‐developed’ social cognition in these conditions. This pattern of findings suggests that human social cognition and behaviour are structured, in part, by joint and opposing effects of oxytocin and testosterone, and that extremes of such joint effects partially mediate risks and phenotypes of autism and psychotic‐affective conditions. These considerations have direct implications for the development of therapies for alleviating disorders of social cognition, and for understanding how such disorders are associated with the evolution of human cognitive‐affective architecture.     

The neurobiology of mammalian parenting and the biosocial context of human caregiving

This article is part of a Special Issue “Parental Care”. Research on the neurobiology of attachment, pioneered by scholars in the generation that followed the discovery of social bonding, examined the biological basis of mammalian parenting through systematic experiments in animal models and their application to theories on human attachment. This paper argues for the need to construct a theory on the neurobiology of human attachment that integrates findings in animal models with human neuroscience research to formulate concepts based on experimental, not only extrapolative data. Rosenblatt's (2003) three characteristics of mammalian parenting – rapid formation of attachment, behavioral synchrony, and mother-offspring attachment as basis of social organization – are used to guide discussion on mammalian-general versus human-specific attributes of parental care. These highlight specific components of attachment in rodents, primates, and humans that chart the evolution from promiscuous, nest-bound, olfactory-based bonds to exclusive, multi-sensory, and representation-based attachments. Following, three continua are outlined in parental behavior, hormones, and brain, each detailing the evolution from rodents to humans. Parental behavior is defined as a process of trophallaxis – the reciprocal multisensory exchange that supports approach orientation and enables collaboration in social species – and includes human-specific features that enable behavioral synchrony independent of tactile contact. The oxytocin system incorporates conserved and human-specific components and is marked by pulsatile activity and dendritic release that reorganize neural networks on the basis of species-specific attachment experiences. Finally, the subcortical limbic circuit underpinning mammalian mothering extends in humans to include multiple cortical networks implicated in empathy, mentalizing, and emotion regulation that enable flexible, goal-directed caregiving. I conclude by presenting a philosophical continuum from Hobbes to Lorenz, which illustrates how research on the neurobiology of attachment can put in the forefront the social-collaborative elements in human nature and afford a new perspective on the mind-brain polarity.     

Genetic and phenotypic variations of inherited retinal diseases in dogs: the power of within- and across-breed studies

Considerable clinical and molecular variations have been known in retinal blinding diseases in man and also in dogs. Different forms of retinal diseases occur in specific breed(s) caused by mutations segregating within each isolated breeding population. While molecular studies to find genes and mutations underlying retinal diseases in dogs have benefited largely from the phenotypic and genetic uniformity within a breed, within- and across-breed variations have often played a key role in elucidating the molecular basis. The increasing knowledge of phenotypic, allelic, and genetic heterogeneities in canine retinal degeneration has shown that the overall picture is rather more complicated than initially thought. Over the past 20?years, various approaches have been developed and tested to search for genes and mutations underlying genetic traits in dogs, depending on the availability of genetic tools and sample resources. Candidate gene, linkage analysis, and genome-wide association studies have so far identified 24 mutations in 18 genes underlying retinal diseases in at least 58 dog breeds. Many of these genes have been associated with retinal diseases in humans, thus providing opportunities to study the role in pathogenesis and in normal vision. Application in therapeutic interventions such as gene therapy has proven successful initially in a naturally occurring dog model followed by trials in human patients. Other genes whose human homologs have not been associated with retinal diseases are potential candidates to explain equivalent human diseases and contribute to the understanding of their function in vision.     

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.     

An overview of types of aggressive behaviour in dogs and methods of treatment

In 223 cases of dogs presented to a specialist behavioural clinic in Brisbane, Australia, 87 (39%) were for severe aggression. The classes of aggression included dominance (31.6%), territorial (29%), predatory (12.3%), intermale (12.3%), sibling rivalry (7.9%), fear biting (6%) and idiopathic rage (0.9%). The breeds most represented which attacked humans were the Bull Terrier (16%), German Shepherd and crosses (15%), Cattle dog breeds (Blue Heeler and crosses, 9.2%), Terrier breeds (9.2%), Labrador (8%), Poodle and Cocker Spaniel (both 5.7%) and Rottweiler (4.6%). The dangerous dog list put out by the local Brisbane City Council includes the first three breeds mentioned and the Rottweiler as the top four breeds causing aggression problems.

Hospital records in Victoria and Queensland confirm that most damage is caused to humans by Bull Terriers and German Shepherds. Many breeds similar to those in our study are also represented in American data on aggressive breeds.

Treatments included obedience training only, restraint only, obedience and restraint, synthetic progestins and obedience, castration, progestins and obedience, castration and obedience, use of chlorpromazine and as a last resort, euthanasia (12.6%). Entire males formed the largest group (44%), followed by castrated males and females (both 21%) and spayed females (15%).

Several breeds (Boxer, Briand, Samoyed and St. Bernard) only attacked other animals and birds.

This study reinforces evidence that social disruption is caused by aggressive dogs, but it also indicates that many responsible clients seek advice on how to deal with this behavioural problem.     

Children and their pet dogs : How they communicate

The research of ethologists has provided a better understanding of the mechanisms, role and development of communication behaviour between young children and their peers. However, little is known about the communication systems between children and their pets. A study of these relational systems would be needed to understand how the child interacts with his whole environment.The present study is based on the analysis of video tapes filmed during spontaneous interactions between children from 2 to 5 years of age with their pet dog (N = 45) in their home environment. Inventories were made of the child and dog behaviours during these interactions. The results have shown the different dog behaviours induced by the child and the different child behaviours induced by the dog. The links between these behaviours and the variables which characterize both partners (age, sex, etc.) were treated by factor analysis of correspondences. These data are discussed in relation to the behavioural inventories of children and dogs with their peers and conspecifics.