The party isn't over yet! Here's another helping of Monday Pets. Enjoy!

Wild Dog crawled into the Cave and laid his head on the Woman's lap... And the Woman said, "His name is not Wild Dog any more, but the First Friend."

--Just So Stories, Rudyard Kipling.

ResearchBlogging.orgArchaeological evidence indicates that dogs were already a part of human society around the end of the Ice Age. Small dog skeletons have been unearthed in human communities as far back as 6- to 12-thousand years ago in Europe, the Middle East, and China. The jawbone of a domestic dog was found in a late Paleolithic grave in Germany, and dated to around 14 thousand years ago. And there is the famous site at Ein Mallaha (Eynan, in Hebrew), in Northern Israel where an elderly human and a 4-5 month old puppy were buried together, 10- to 12-thousand years ago.

ein mallaha.jpg

Figure 1: From the site at Ein Mallaha. The person's left hand is placed on the body of a 4-5 month old puppy.

Some evidence exists that dogs were the first animals to be domesticated, and until now, humans have only succeeded in domesticating around 20 different animal species. Compared with those other species (such as sheep, goats, pigs, cows, horses, donkeys, and camels), only dogs (and to some extent, cats, though at the risk of alienating readers, I maintain that cats are evil) have established for themselves a social niche within human society. Dogs were not only bred for companionship; some dogs were bred for hunting, guarding, or herding. More recently, dogs have worked as service dogs or drug-sniffing dogs. The question remains: Why do dogs have such apparent psychological effects on humans?

One hypothesis claims that humans develop positive feelings and behaviors towards dogs as a side-effect of a mechanism in place that forms the bond between parents and children. Attachment, or social bonding, is a sort of behavioral regulation system that exists to reduce the risk of harm (e.g. predation) to a young animal.

John Bowlby described two characteristics of the attachment relationship in mammals and birds:

(1) Parents maintain physical proximity to their young (and the young to their parents), and if that proximity is broken, they strive to restore it.

(2) Parents and their young display special behavior towards each other that they would not display towards others of their species. Parent-child relationships are specific, and characterized by individual recognition and differential behavior.

Most studies of dog-human attachment have relied on psychological scales and questionnaires. One group of researchers, however, from Azabu University in Japan, have attempted to provide a biological perspective to this question.

They begin with the assumption that individual recognition is essential for long-term bonds between between individuals. This is not as trivial as it sounds. Human adults are extraordinarily bad at distinguishing among monkey faces, for example, though highly skilled at distinguishing among human faces.


Figure 2: I promise, those monkey faces belong to different individuals.

Previous research showed that dogs are able to discriminate between human beings, and they're able to do it in a multimodal way, combining both visual and auditory stimuli. For example, they tend to look longer at a picture of their owner when it is paired with a recording of their owner's voice than with a stranger's voice. Other research has demonstrated that both human infants and dogs, but not human-reared wolves, behaved differently with strangers than with their owners (or parents). Is there a physiological mechanism that underlies this behavioral pattern?

Under normal resting conditions, the heart rate (HR) shows regular variation in beat-to-beat intervals. This variation is referred to as heart rate variability, or HRV. In dogs, HR increases during periods of increased physical activity (as would be expected), but HRV increased when dogs were playing with their favorite toy. So while HR is a measure of activity, HRV may indicate attention. The ratio of the low frequency part of the HRV pattern to the high frequency part is considered to reflect the activity of the autonomic nervous system.

Seven adult dogs and their owners participated in the study. The dog was put into an enclosure, and then presented with three strangers and their owner. Each of the strangers was of the same sex and of similar appearance to the owners. Each individual (the three strangers and the owner) were present for 4 minutes each, with 3 minute intervals between them. HR and HRV were measured during each stimulus presentation.

They found that HR and HRV decreased significantly between the first stranger and the third stranger, and this was probably due to habituation; the dog became used to seeing strangers. Then, when the owner was presented, HR and HRV both significantly increased.


Figure 3: HR when presented with strangers 1-3, and then the owner (top). HRV when presented with strangers 1-3, and then the owner (bottom).

As you can see, the difference in HR and HRV between strangers 1 and 3 is significant, as are the differences in HR and HRV between stranger 3 and the owner. This means that not only do dogs discriminate between their owners and other humans, but they also display an emotional response towards them (as indicated by the autonomic arousal). So at least one of the criteria for attachment, individual recognition, is fulfilled.

When a social bond is broken, animals exhibit separation anxiety (I have scratch marks on my door to prove it) and a stress response in the endocrine system is activated. It is important to differentiate this form of attachment-based social bonding from a more general form of social affiliation. When separating monogamous animal pairs, separation anxiety and the endocrine response both occur. But separation of mates in a polygamous species does not elicit the physiological endocrine response.

Oxytocin is a hormone that occurs in the brain, and is important for bonding between mating pairs and between parents and children (Sci has covered oxytocin exhaustively, if you're interested). Increases in oxytocin levels are implicated in infants' memory formation of their caregiver, and in the process of pair-bond formation in monogamous species (like prairie voles). If you give prairie voles a drug that blocks oxytocin just before mating, the pair-bond won't form. Oxytocin given to stressed out animals (humans included) will cause them to relax, and cope with the stress. Oxytocin has even been called "the most important neurotransmitter that is responsible for social bonding." So you might expect oxytocin to figure prominently in the human-dog relationship.

Fifty-five human dog owners participated in this experiment, and all answered a brief questionnaire regarding their relationship with their dogs.

Experimental condition: First the owner pees into a cup. Then they play with their dogs for half an hour. Then they pee into a cup again.

Control condition: First the owner pees into a cup. Then they are made to sit facing a wall, and not interact with their dogs for half an hour. Then they pee into a cup again.

Then the experimental group was split in half on the basis of how long their dogs looked at them while playing. There was a strong correlation between gaze duration and the strength of the relationship, as assessed by the questionnaire.

And guess what? Those in the experimental group who had stronger relationships with their dogs also had more oxytocin in their urine, compared with the other group, who reported weaker relationships with their dogs! So the initial hypothesis, that the human-dog relationship emerges out of a mechanism initially designed to stimulate and maintain the parent-child relationship, may indeed be supported!

The changes in HRV as well as attenuation of oxytocin are both probably related to activity of the hypothalamic-pituitary-adrenal, or HPA, axis (which is involved, among other things, in the stress response).

There's still a lot left to figure out, but this study was a pretty important piece of the puzzle. It provides a clue as to the neural mechanisms that support the relationship between dogs and humans. It may also suggest a physiological mechanism to account for anecdotal reports of health-related benefits following animal interaction, but a lot more research is needed for that. It may also be the case that the attachment system in both humans and dogs share a similar neurophysiological mechanism (via the HPA axis). That may explain why dogs have adapted so easily to human society, and why humans so readily treat dogs as part of the family.

Nagasawa, M., Mogi, K., & Kikusui, T. (2009). Attachment between humans and dogs Japanese Psychological Research, 51 (3), 209-22.1 DOI: 10.1111/j.1468-5884.2009.00402.x