“Are you all right?” I asked.
He waved me off. “I just need to get some air.”
By now, the excitement of parading the dogs across the quad to the hospital had worn off, and only lab members who actually had a job to do on the Dog Project accompanied us. I still got a thrill out of the walk, though.
Like a well-oiled machine, everyone took up their positions at the scanner. Melissa and McKenzie were there, of course, and they relaxed in the control room until it was their turn. Andrew set up a test-tube rack on a plastic worktable at the rear of the magnet. He inserted the cotton swabs, business end down, in each tube.
For each dog, Andrew had prepared seven swabs: the four combinations of strange and familiar humans and dogs, plus an intermediate category of “acquaintances.” Callie and McKenzie were acquaintances. They knew each other, but there was no reason to expect that they viewed each other as part of their pack. We would present their scents to each other for this category. In this fashion, we would have a continuum of familiarity from stranger to acquaintance to household member. Using lab members’ sweat, we created the corresponding human acquaintance category. Finally, for a baseline, we used the dogs’ own urine as a “self” category.
With Callie in the scanner, the shimming and localizer sequence took less than a minute. She knew the routine. For the functional scans, we modified the hot dog experiment. Instead of holding up a hand signal for ten or fifteen seconds, Andrew would hand me a swab, and I would hold it in front of Callie’s nose for a few seconds. She would continue holding still to allow enough time for the hemodynamic response to peak, and then I would reward her with a hot dog treat. It was the same as before except we would insert a smell during the middle of the repetition.
To get her used to a cotton swab being shoved in front of her face, Callie and I had practiced this at home. The first few times she backed away, but she soon realized nothing bad was going to happen and just sniffed.
With the functional scans running, she performed flawlessly. Each swab was presented eight times in random order. It took two functional runs lasting six minutes each, and then we were done. Another four hundred scans in the can.
McKenzie, on the other hand, was not having a good day. She did not like the smells or the swabs coming at her. From the control room, I could see that her brain images were moving. Even though we acquired nearly five hundred images, most were unusable. She would have to come back another day after more training with the swabs.
Like we did in the hot dog experiment, Andrew and I analyzed the smell data individually for the two dogs as well as combining their brains. Both analyses yielded surprising results. When we combined their brains, we were able to identify the parts of the brain that reacted to the different smells in both dogs. This showed the common regions of activation. In contrast, the individual analyses told us how the dogs reacted differently. We focused on two comparisons.
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?