The role of oxytocin in relationships between dogs and humans and potential applications for the treatment of separation anxiety in dogs

The hormone oxytocin plays an important role in attachment formation and bonding between humans and domestic dogs. Recent research has led to increased interest in potential applications for intranasal oxytocin to aid with the treatment of psychological disorders in humans. While a few studies have explored the effects of intranasally administered oxytocin on social cognition and social bonding in dogs, alternative applications have not yet been explored for the treatment of behavioural problems in this species. One potentially important application for intranasal oxytocin in dogs could be the treatment of separation anxiety, a common attachment disorder in dogs. Here we provide an overview of what is known about the role of oxytocin in the human–dog bond and canine separation anxiety, and discuss considerations for future research looking to integrate oxytocin into behavioural treatment based on recent findings from both the human and dog literature.     

The Precultural Basis of the Incest Taboo: Toward a Biosocial Theory

The literature on the origins of the incest taboo is characterized by controversy over the nature/nurture issue, and fears of reductionism. In recent years work emanating from such diverse disciplines as cultuml and physical anthropology, ethology, and neuropsychology warmnts a new look at this intriguing issue. It is probable that incest avoidance is widespread among the vertebrata and is "built into the wiring." As learned behavior becomes more important phylogenetically, curiosity and exploration plays a larger role in adaptation and has manifest survival admntages. Incest awidance functions as a mechanism to propel the individual into new relationships and "social territory." For humans, incest avoidance and its later elaboration into a cultuml taboo serve to motivate exploration of and attachment to a wider social nexus than the family. It also prevents fixation at a relatively undifferentiated psychological stage of development     

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.     

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.     

Choosy moral punishers

The punishment of social misconduct is a powerful mechanism for stabilizing high levels of cooperation among unrelated individuals. It is regularly assumed that humans have a universal disposition to punish social norm violators, which is sometimes labelled "universal structure of human morality" or "pure aversion to social betrayal". Here we present evidence that, contrary to this hypothesis, the propensity to punish a moral norm violator varies among participants with different career trajectories. In anonymous real-life conditions, future teachers punished a talented but immoral young violinist: they voted against her in an important music competition when they had been informed of her previous blatant misconduct toward fellow violin students. In contrast, future police officers and high school students did not punish. This variation among socio-professional categories indicates that the punishment of norm violators is not entirely explained by an aversion to social betrayal. We suggest that context specificity plays an important role in normative behaviour; people seem inclined to enforce social norms only in situations that are familiar, relevant for their social category, and possibly strategically advantageous.     

Oxytocin and social affiliation in humans

A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and behavioral responses of attachment partners during social contact is presented as a theoretical and empirical framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) system provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is stable over time within individuals, is mutually-influencing among partners, and that mechanisms of cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing links between peripheral and genetic markers of OT with concurrent parenting and memories of parental care; between administration of OT to parent and infant's physiological readiness for social engagement; and between neuropeptides and the online synchrony of maternal and paternal brain response in social-cognitive and empathy networks support the hypothesis that human attachment develops within the matrix of biological attunement and close behavioral synchrony. The findings have conceptual implications for the study of inter-subjectivity as well as translational implications for the treatment of social disorders originating in early childhood, such as autism spectrum disorders, or those associated with disruptions to early bonding, such as postpartum depression or child abuse and neglect. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Re-Evaluating Primate Monogamy

Researchers propose hypotheses for the occurrence of monogamy as a social system in primates based on the assumption that there are a group of primates, including humans, which live exclusively in "nuclear families" and share a similar set of social behaviors. Examining the primates purported to be "monogamous" reveals that they cover a wide range of grouping types, mating patterns, taxonomic groups, and evolutionary grades. While there are a few primate species that do live in small, two-adult groups and share a similar set of social behaviors, the vast majority of the supposed "monogamous" primates, including humans, do not. [monogamy, social systems, evolution, variability in social organization]     

Holographic imaging of unlabelled sperm cells for semen analysis: a review

Male reproductive health in both humans and animals is an important research field in biological study. In order to characterize the morphology, the motility and the concentration of the sperm cells, which are the most important parameters to feature them, digital holography demonstrated to be an attractive technique. Indeed, it is a label‐free, non‐invasive and high‐resolution method that enables the characterization of live specimen. The review is intended both for summarizing the state‐of‐art on the semen analysis and recent achievement obtained by means of digital holography and for exploring new possible applications of digital holography in this field.

Quantitative phase maps of living swimming spermatozoa.     

Hierarchy

Dominance hierarchies (sometimes called “pecking orders”) are virtually universal in social species, including humans. In most species and in ancestral and early human societies, these hierarchies allocate scarce resources, including food and often access to females. Humans sometimes use hierarchies for these allocational purposes, but humans use hierarchies for productive purposes as well—as in firms, universities, and governments. Productive hierarchies and dominance hierarchies share many features. As a result, people, including students of human behavior, often confuse types of hierarchies. For example, the Communist Manifesto attributes features to productive hierarchies that are actually characteristic of dominance hierarchies. Government hierarchies are particularly confusing, as they have many features of both types. In modern societies with socially mandated monogamy and voluntary attachment to hierarchies in the form of competitive labor markets, productive hierarchies are generally useful for all members, and it is important not to confuse the two types, either in policy or in scientific analysis.     

Human infections due to nematode helminths nowadays: epidemiology and diagnostic tools

An update on the epidemiology of intestinal and tissue roundworms, in the world as well as in Italy, is presented. This analysis indicates that the most important changes happened in developed countries, where two main phenomena have been registered. The improvements occurred in social, economic, hygienic and sanitary conditions resulted in decrease of intestinal geohelminth prevalence but, besides, the changes happened at level of other factors, like environment, climate and human behaviour, promote more and more the opportunity for infections due to animal nematode species, which in people induce tissue syndromes. Therefore, the easier circulation of zoonoses among humans constitutes the main remark, which has to be strongly taken into account in countries like Italy, in that it is an emerging sanitary problem, important both for the number of people involved, and for the difficulties induced by their diagnosis. The general trend of "traditional" and "new" nematode infections that can affect humans is analysed, changes in the distribution patterns are tentatively explained, and available diagnostic tools are summarised.     

The Way to a Man's Heart Is through His Stomach: What about Horses?

Background

How do we bond to one another? While in some species, like humans, physical contact plays a role in the process of attachment, it has been suggested that tactile contact''s value may greatly differ according to the species considered. Nevertheless, grooming is often considered as a pleasurable experience for domestic animals, even though scientific data is lacking. On another hand, food seems to be involved in the creation of most relationships in a variety of species.

Methodology/Principal Findings

In this study, we used the horse training context to test the effects of food versus grooming during repeated human-horse interactions. The results reveal that food certainly holds a key role in the attachment process, while tactile contact was here clearly insufficient for bonding to occur.

Conclusion/Significance

This study raises important questions on the way tactile contact is perceived, and shows that large inter-species differences are to be expected.     

Oxytocin receptors modulate a social salience neural network in male prairie voles

Social behavior is regulated by conserved neural networks across vertebrates. Variation in the organization of neuropeptide systems across these networks is thought to contribute to individual and species diversity in network function during social contexts. For example, oxytocin (OT) is an ancient neuropeptide that binds to OT receptors (OTRs) in the brain and modulates social and reproductive behavior across vertebrate species, including humans. Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior. In voles, OTR density in the nucleus accumbens (NAc)—a region important for social and reward learning—is associated with individual and species variation in social attachment behavior. Here we test whether OTRs in the NAc modulate a social salience network (SSN)—a network of interconnected brain nuclei thought to encode valence and incentive salience of sociosensory cues—during a social context in the socially monogamous male prairie vole. Using a selective OTR antagonist, we test whether activation of OTRs in the NAc during sociosexual interaction and mating modulates expression of the immediate early gene product Fos across nuclei of the SSN. We show that blockade of endogenous OTR signaling in the NAc during sociosexual interaction and mating does not strongly modulate levels of Fos expression in individual nodes of the network, but strongly modulates patterns of correlated Fos expression between the NAc and other SSN nuclei.     

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.     

Neuroactive hormones and interpersonal trust: International evidence

Social attachment is vital for human health and welfare. Recent experimental evidence in humans has identified the role of neuroactive hormones, especially the peptide oxytocin, in mediating trusting behaviors. Herein, we test if the endocrinological basis for trust between humans scales up to the country level. Trust pervades nearly every aspect of our daily lives, yet survey data on trust show substantial variation across countries. Using 31 measures of biological, social, and environmental factors associated with hormone levels for a sample of 41 countries, we find that two classes of factors are related to trust: consumption of plant-based estrogens (phytoestrogens), and the presence of environmental conditions that include measures of estrogen-like molecules. Our findings provide preliminary evidence that interpersonal trust at the country level may be related to the intake of neuroactive hormones.     

NCK is critical for the development of deleted in colorectal cancer (DCC) sensitive spinal circuits

As our understanding of motor circuit function increases, our need to understand how circuits form to ensure proper function becomes increasingly important. Recently, deleted in colorectal cancer (DCC) has been shown to be important in the development of spinal circuits necessary for gait. Importantly, humans with mutation in DCC show mirror movement disorders pointing to the significance of DCC in the development of spinal circuits for coordinated movement. Although DCC binds a number of ligands, the intracellular signaling cascade leading to the aberrant spinal circuits remains unknown. Here, we show that the non‐catalytic region of tyrosine kinase adaptor (NCK) proteins 1 and 2 are distributed in the developing spinal cord. Using dissociated dorsal spinal neuron cultures we show that NCK proteins are necessary for the outgrowth and growth cone architecture of DCC^+ve dorsal spinal neurons. Consistent with a role for NCK in DCC signaling, we show that loss of NCK proteins leads to a reduction in the thickness of TAG1^+ve commissural bundles in the floor plate and loss of DCC mRNA in vivo. We suggest that DCC signaling functions through NCK1 and NCK2 and that both proteins are necessary for the establishment of normal spinal circuits necessary for gait.

     

The effect of peer separation in young chimpanzees (Pan troglodytes)

Ten chimpanzees (Pan troglogytes), aged 18–24 months, housed without mothers as two dyads and two triads, were subjected to social separation. Two issues were addressed: the effects of peer separation in chimpanzees; and differential responses by subjects living in dyads compared with those living in triads. Chimpanzees that were alone during separation reacted with high levels of “protest” alternating with “despair” throughout the separation period. The continued presence of one cagemate, during separation from a third, was a strong mitigating factor. Even when the primary attachment was formed with the absent cagemate, the remaining chimpanzees clung to each other and the levels of protest and despair, when present, were low. Upon reunion, neither “detachment” nor heightened levels of clinging were conspicuous, but there was increased social interaction. The data on separation of chimpanzees are intermediate between those of humans and monkeys separated from mothers or peers. The increased social interactions during reunion, including looking, are comparable to the visual vigilance reported for humans.     

Mental rehearsal in great apes (Pan troglodytes and Pongo pygmaeus) and children

The ability to rehearse possible future courses of action in the mind is an important feature of advanced social cognition in humans, and the "social brain" hypothesis implies that it might also be a feature of primate social cognition. We tested two chimpanzees, six orangutans and 63 children aged 3-7 years on a set of four puzzle boxes, half of which were presented with an opportunity to observe the box before being allowed to open it ("prior view"), the others being given without an opportunity to examine the boxes before handling them ("no prior view"). When learning effects are partialled out, puzzle boxes in the "prior view" condition were opened significantly faster than boxes given in the "no prior view" condition by the children, but not by either of the great apes. The three species differ significantly in the speed with which they opened boxes in the "no prior view" condition. The three species' performance on this task was a function of relative frontal lobe volume, suggesting that it may be possible to identify quantitative neuropsychological differences between species.     

Lust, attraction, and attachment in mammalian reproduction

This paper proposes that mammals exhibit three primary emotion categories for mating and reproduction: (1) the sex drive, or lust, characterized by the craving for sexual gratification; (2) attraction, characterized by increased energy and focused attention on one or more potential mates, accompanied in humans by feelings of exhilaration, “intrusive thinking” about a mate, and the craving for emotional union with this mate or potential mate; and (3) attachment, characterized by the maintenance of close social contact in mammals, accompanied in humans by feelings of calm, comfort, and emotional union with a mate. Each emotion category is associated with a discrete constellation of neural correlates, and each evolved to direct a specific aspect of reproduction. The sex drive is associated primarily with the estrogens and androgens; it evolved to motivate individuals to seek sexual union. The attraction system is associated primarily with the catecholamines; it evolved to facilitate mate choice, enabling individuals to focus their mating effort on preferred partners. The attachment system is associated primarily with the peptides, vasopressin, and oxytocin; it evolved to motivate individuals to engage in positive social behaviors and assume species-specific parental duties. During the evolution of the genus Homo, these emotion systems became increasingly independent of one another, a phenomenon that contributes to human mating flexibility and the wide range of contemporary human mating and reproductive strategies.     

Effect of gentle nursing care of premature infants on bonding and emotional development of the child. Follow-up of premature infants in Dr. Marina Marcovich's study

The study was set out to investigate whether the Marcovich model of a "soft treatment" of premature infants encourages the parent-infant-relationship to such an extent that, at school age, the Marcovich-children would be found to differ significantly from children treated with standard care with regard to the quality of their attachment and the prevalence of emotional and behavioural disorders. The Marcovich-children of the present sample had been discharged from hospital much earlier than the standard group, they were less frequently treated with artificial respiration, infant-parent body contact was encouraged significantly earlier, and, although they were less frequently breast-fed, those who were breast-fed were allowed to do so at a much earlier stage. The Marcovich-children were found to display higher social competence, more emotional openness, more emotional coherence, less dismissal of attachment and less preoccupied anger. The two samples did not differ with regard to their total attachment quality as well as their emotional and behavioural problems. The fact that no significant differences could be established with regard to the quality of the attachment suggests that the complex life-saving attachment system is not irreversibly affected by the early separation and distress and that the months and years after the hospital stay have the power to make up with any experienced trauma. It seems, however, that special aspects of the attachment system, such as the communication and interaction, are positively encouraged and enhanced by the soft treatment of the premature infant, which leads to greater emotional openness and social competence, as well as less preoccupied anger against the attachment figures.     

Insights from social transmission of information in rodents

Direct exposure to stimuli in their environment is not the only way that animals learn about important information. Individuals can infer fear from a social context through observation. Like humans, rats are very social animals, and may learn to infer information about their environment through their interactions with conspecifics. Here, we first review different models for social transmission of information in rodents. Second, we examine different modes of communication that are important to social learning. Then, we cover the different proximate factors that are thought to modulate the social transmission of information. Next, we identify social and environmental conditions that impact social learning, and finally, we conclude by revisiting social transmission through the lens of the Tinbergen framework.