First, we compared the brain activity of dog scents to human scents. This was done by ignoring whether the scent was familiar or strange. We simply averaged all the dog scents together and all the human scents together and compared the two brain patterns. The first thing that popped out was that the canine smells strongly activated the olfactory bulb and the frontal cortex above it. I suspected that this was because dog urine is a more potent stimulus than human sweat.

When we compared the familiar scents to the strange scents, ignoring whether it was from a dog or a human, once again, we found more activation of the olfactory regions to the strange smells. This demonstrated that the olfactory activation is controlled not just by the potency of the smell but also by its familiarity. Familiar smells don’t require much brain processing. Strange ones do. Consistent with this interpretation, the dogs’ own urine didn’t evoke any detectable brain activity. Just like humans aren’t aware of the smell of their own breath, dogs seem to tune out the smell of their own pee.

Strangely, we also observed strong activation to the unfamiliar smells in the cerebellum, a part of the brain usually associated with movement. When I was presenting the cotton swabs to Callie, sometimes she sniffed more intensely. The cerebellum activation was most likely the neural origin of the sniffing, which would be more intense for smells the dogs hadn’t encountered.

The most interesting finding appeared when we subdivided the dog and human scents into their subcategories of familiar and unfamiliar. One, and only one, type of smell activated the caudate: familiar human. This was especially true for Callie. In her case, the familiar human was Kat.

Kat’s sweat activated Callie’s caudate—same as the signal for hot dogs. But Kat wasn’t even at the scanner. This meant that Callie had identified the scent as Kat even though she wasn’t physically present. And if Callie had a mental category for Kat that didn’t require her physical presence, then this suggested that Callie had a sense of permanence for the people in her household. She knew who her family was, and she remembered them. We found further evidence for this interpretation in an area called the inferior temporal lobe. This part of the brain is closely associated with memory function, and like the caudate, the inferior temporal lobe was strongly activated by the smell of a familiar human.

The inferior temporal activation told us that the dogs remembered their human family, and the caudate activation, more prominent in Callie, told us that her remembrance of Kat was a positive one. Could it be longing? Or love? It seemed entirely possible. These patterns of brain activation looked strikingly similar to those observed when humans are shown pictures of people they love.

The results of the smell experiment expanded our understanding of the dogs’ mental world. All through the Dog Project, we had been focused on the nature of the dog-human relationship. We love dogs, but what do they think of us? Even with just two dogs, a picture was beginning to emerge. The pattern of activations in the cortex suggested that they concocted mental models of our behavior, which might be due to mirror neuron activity. But regardless of the mechanism, the smell data showed that their mental models included the identity of important people in their lives that persists even when the people aren’t physically present.

I was willing to accept that as an acceptable demonstration of love from Callie. But even if I was being too generous, the fact that the dogs knew who we were, and that they had categories for us, indicated that we humans make a lasting impression on our dogs. We are appreciated.

22

First Friend

WHEN WE BEGAN THE DOG PROJECT, we had no idea what we would find. What started as a half-baked idea to scan dogs’ brains mushroomed into a full-fledged research program faster than I ever expected. Even with just hot dogs, and then smells, we had found evidence that dogs mentalized about the humans in their lives. I suppose this should not have been surprising. Many dog owners are convinced that their dogs know who they are and return their love for them. But, for the first time, we saw direct evidence of reciprocation in the dog-human relationship and social cognition in the canine brain.

This was truly exciting, but, in the interest of scientific objectivity, we had to be careful in generalizing from our experiments. The World Health Organization estimates that the population of dogs is 10 percent that of humans. That translates into roughly 700 million dogs worldwide. And we had studied the brains of precisely two of them. Although we had expanded the enrollment in the Dog Project since our initial experiments, we were still studying a very selective group of dogs. These were dogs that were loved by their humans. But even that is not enough. Most dogs aren’t willing to go into an MRI, and most people aren’t willing to train them to do so. That still leaves the 700 million dogs of the world. What did our experiments tell us about those dogs and their relationships to humans?

From an evolutionary perspective, dogs are incredibly successful. Their numbers speak to that. Given that dogs share their environmental niche with humans, their success must be a result of learning how to read us. Not just reading human behavior but, I believe, learning to read our intentions, which means that they have a theory of mind for humans. And that is exactly what we found in the Dog Project. So even though Callie and McKenzie were rarified representatives of the world dog population, what we found in their brains showed the defining characteristic of dogs: social learning. Their brains showed that they cared about human intentions.

Proof of social cognition means that dogs aren’t just Pavlovian learning machines. It means that dogs are sentient beings, and this has startling consequences for the dog-human relationship.

Most of the dogs in the world are village dogs. They are not anyone’s pets, although they might look that way at first glance because they often gather near humans. People know who the dogs are, but they might not have names. Village dogs insinuate themselves into the fabric of human societies. They feed on scraps, sometimes garbage, and sometimes food that is deliberately left by humans for them to eat. In some parts of the world, people let them hang around just so that they can eat them later.

If Callie had lived anywhere else in the world, she would have been a village dog. She had that rangy appearance—not too big, not too small—and the eyes of an opportunist. For the first year that she lived in our house, I was convinced that she would run away at the first opportunity of something better. But after the Dog Project, I no longer thought that. The project had changed both her brain and mine.

Indeed, if there is one thing dog ethologists can agree on (and it might indeed be only one thing), dogs are masters of change. If nothing else, dogs’ defining characteristic is their adaptability. Apart from vermin, dogs are the only mammalian species that is found everywhere humans are, and humans have occupied every habitable niche on the planet. As the ethologists Raymond and Lorna Coppinger observed, “The rapidity with which the dog has changed form, and the seemingly endless varieties of its form, challenge the theory of Darwinian evolution, that adaptation must be a slow process.” The Coppingers were referring primarily to dogs’ changing physical form, but the same can be said for dogs’ behavior.