I was relieved that we had Callie back. The episode made me realize that despite all of our high-tech training for the MRI, I still didn’t have a clue as to what she was thinking.
By the time we got home, Callie had already shrugged off her trip downriver, and the kids had taken to exercising their creativity on the stack of boogie boards in the basement. The nearest ocean was three hundred miles away, so something else had to substitute for water. It didn’t take them long to figure out that sliding down the carpeted steps was a hoot.
Helen and Maddy laid out pillows at the bottom of the steps. In rapid fire, they placed a board at the top of the stairs and went shooting down into the pillow pit. Of course, this was highly exciting to Callie and Lyra. Callie zoomed up and down the stairs trying to catch the kids as they went tumbling past. As Callie chased the girls, she made a huuuf-huuuf-huuuf sound that sounded a lot like a person trying not to laugh. Lyra just stayed at the bottom of the stairs, barking incessantly. A strand of drool stretched to the floor.
When the girls got tired of stair surfing, they used the boogie boards as shields while play jousting in the basement. When they got tired of that, they just started whacking each other.
“Daa-ad!” someone yelled. “She broke one of your boogie boards!”
I ventured into the melee. Sure enough, one of the boards had snapped into two pieces. Callie was in a sphinx position on the floor, swishing her tail, and looked up at me with an I-didn’t-do-it expression on her face. Lyra, who was chewing on one of the chunks, had taken a bite out of one of the pieces and was about to swallow it when I reached into her mouth and swept it away. I picked up the board and stared at the crescent she had made. It was about the size of Callie’s chin.
A lightbulb went off in my head.
I retrieved a utility knife from the garage and cut the broken boogie board into strips. Carefully, I began carving out a semicircle on the edge of each piece. After each pass, I would check the fit against Callie’s chin. The first piece had a small cutout for the end of her muzzle. The next piece had a bigger cutout, and the next bigger yet. Stacked against each other, the cutouts were beginning to form a three-dimensional cradle. The fourth piece was the biggest. A deep cutout allowed the foam to extend up to Callie’s ears and fit behind the back of her jaw. This provided a secure support both up and down and, crucially, forward and backward.
With the sandwich of four pieces taped together, I checked the fit on Callie. She had retired to the sofa. Gently, I lifted up her head and placed the foam sandwich beneath her chin. She relaxed and looked at me with indifference.
I was ecstatic. I snapped some photos to send to Andrew and Mark. The new chin rest would solve our motion problems. It was firm, so it would support the weight of Callie’s head and prevent movement up and down. But the cutout also provided her with positive feedback on where to place her head. Her chin would fit in only one way, and the cutout guaranteed that as long as Callie nestled her head down into it, the location would be the same left to right and front to back.
Callie testing the fit of the boogie board chin rest.
(Gregory Berns)
The next day, I trimmed up the foam block and glued it to a piece of plywood that would span the diameter of the head coil. The plywood was cut to just the right length so that the whole chin rest placed Callie’s head in the center of the coil while allowing space beneath it for her paws to stick forward.
With the contraption on the floor, I called to Callie, “Coil!”
She scooted in and immediately plopped her head in the rest.
“Excellent!” I exclaimed, and gave her a piece of hot dog. She happily swallowed it and placed her head back down. She waited for more.
Next, we tried it with the earmuffs. Callie still didn’t like them, but with enough hot dogs, I coaxed her into the coil while wearing the muffs. I tapped the new chin rest, and she dutifully placed her head in the cradle. The muffs slipped back a little, but I was able to slide them forward again over her head. Callie’s eyes dilated as she anticipated treats.
“You are such a good dog!”
Callie appeared so comfortable in the new chin rest that I began lengthening the time she had to stay motionless before giving her a treat. In a dozen repetitions, she was holding absolutely still for up to ten seconds at a time. That was more than enough. We would be able to get at least five full scans of her brain in that period.
The new chin rest design looked very promising. I had already booked the MRI for Dog Day, which was now less than two weeks away. The scanner was reserved for four hours to allow us plenty of time to let the dogs get comfortable in the scanner, but at $500 an hour, this was going to be an expensive experiment. Of course, we wouldn’t know if it was successful until we actually tried it at the scanner. The new chin rest was the best shot we had, so I made one for McKenzie too.
The full monty: Callie in the final version of the chin rest.
(Gregory Berns)
Both dogs made rapid progress with the new chin rest. McKenzie, of course, was already a champ at holding still. The new rest also made it easy for the dogs to consistently place their heads in the same location. There was only one last detail to work out before scan day.
What, exactly, was the scientific question we hoped to answer by scanning dog brains?
14
Big Questions
WITH THE NEW CHIN RESTS, Callie and McKenzie were cruising along in their training. I was routinely blasting the scanner noise at 90 decibels, and as long as Callie had the earmuffs on, she didn’t seem to mind. Scan day was two weeks away. Andrew had circled the date on the lab calendar and written “Dog Day” in bold red letters.
None of us expected to pull off a complete scientific experiment on the first try, so we held on to modest expectations. The first and most important goal of the scan session would be the acquisition of a sequence of fMRI images that weren’t contaminated by motion artifacts. I would consider the session a success if we obtained ten images in a row without the dog moving. That would mean holding still for a twenty-second interval in the scanner. Considering how well the dogs were doing in their training, that seemed entirely possible.
On the off chance that the dogs surpassed our expectations and miraculously held still for several minutes, we would then have the opportunity to collect enough data to go beyond simply proving the viability of the Dog Project. We might actually get to answer a scientific question about canine brain function, which, of course, was the whole point. I didn’t expect to be able to do this on the first go, but it’s always best to be prepared.
I called a meeting of the core Dog Project team—Andrew, Mark, and me—but since everyone in the lab was rooting for this, it turned into an impromptu lab meeting.
“We’ve got two weeks until Dog Day,” I began, “and we have to nail down the experimental task that the dogs will do.”
Because the scanner noise was so loud, the dogs would not be able to hear vocal commands. That left hand signals as the primary means of communication while in the scanner. Up until now, we had purposely avoided using hand signals because we didn’t know what kinds of signals we would use and what the dogs should do with them. It was time to figure that out.
“Not much is known about the functional organization of the dog brain,” Andrew said. “We don’t even know what parts of the dog brain are responsible for basic functions like vision and hearing.” What we did know came from some unsavory experiments over a century old. In 1870, a pair of German scientists used the then new technology of electrical energy to directly stimulate the brains of animals. By sticking their electrodes in different parts of the brain, they discovered that the electricity could cause an animal to move its limbs. Sadly, they used dogs for this experiment, even puppies—a trend that continued into the 1970s. The end result of this research was the knowledge of which parts of the dog brain controlled movement. But for the Dog Project, we couldn’t study the parts of the brain that controlled movement be
cause the dogs weren’t supposed to move!
“Let’s go with our strength,” I said. “Our lab has spent the last decade studying the human reward system. We know a lot about how it works. There isn’t any reason to expect the dog’s reward system to be any different from the human one.”
“Reward-prediction error experiment?” Andrew asked.
The brains of all animals appear to act as prediction engines. Prediction, after all, is key to survival. If your brain weren’t predicting what would happen next, you wouldn’t be able to walk across the street without being hit by a car. Most of the brain’s predictions have to do with things in our environment, like cars, and things that other people are doing. The caudate nucleus (located within the basal ganglia) and the parts of the brain that feed into it are concerned with predicting rewards.
In the early 1990s, Wolfram Schultz, a Swiss neuroscientist, measured the activity of neurons in monkeys’ brains while they were trained on a simple classical conditioning task. When a light turned on in a monkey’s cage, it received a squirt of fruit juice in its mouth. Just like Pavlov’s dogs, the monkeys quickly began to anticipate the juice when the light came on. Schultz discovered that the neurons in specific parts of the brain followed the same pattern. Initially the neurons fired in response to the juice, but once the monkeys had learned the association with the light, the neurons fired to the light, not the juice. The neurons that showed this pattern were located in the heart of the reward system, the caudate.
Since Schultz’s discovery, neuroscientists have learned that these neurons don’t signal things that are pleasurable. Instead, they fire when something unexpected occurs that indicates something good is about to happen. If something is unexpected, then that means the brain made an “error” in predicting it. For this reason, scientists call these events reward-prediction errors.
We know where reward-prediction errors occur in the brains of monkeys and humans. Dogs, we figured, should be no different. And because the caudate is a well-defined structure, it made sense that we would be able to identify it in the dogs’ brains—assuming, of course, they held still for the MRI.
“We could train the dogs with a hand signal that indicated they would receive a hot dog,” I said.
“If the dogs learned the association between the hand signal and the treat,” Andrew agreed, “we should see caudate activity to the hand signal.”
“Just like Schultz’s monkeys,” I concluded.
Lisa spoke up and pointed out a flaw in this reasoning.
“How would you know that the dogs had learned the hand signal?” she asked. “After all, they’re not doing anything.”
She had a point. All of behaviorist learning theory depended on the manifestation of either a response, like drooling, or a behavior to indicate that the animal has actually learned something. We would have only the brain.
“We’ll have to rely on the dogs’ caudate,” I said. “A response there would be proof that they learned the signal. We could also look for other signs, like the pupils dilating in anticipation.”
There was another problem. An fMRI scan measures brain activity indirectly. What it actually measures are changes in the oxygen content of tiny blood vessels in the brain. When neurons fire, the surrounding blood vessels expand a little and let in more fresh blood for the neurons to replenish their energy storage. The scan picks up these changes in blood flow, and from that we deduce which neurons were active. But there is a catch. The brain is always on. It is a myth that we use only some small percentage of our brains. The truth is that we use all of it—just not all at once. Because the brain is always on, and blood is always flowing, fMRI can measure only changes in activity. When designing fMRI experiments, you always need a comparison, or baseline, condition.
Callie would be in the scanner, holding her head still and watching me. So many things could be going on in her brain there might not be a way to interpret the fMRI measurements. Even if we trained the dogs on a hand signal, we would still need something to compare their brain responses to. Ideally, the comparison condition would be almost the same as the thing of interest. You want to keep everything the same in both conditions except for the one thing that is being varied in the experiment.
To measure the response to a hand signal, we needed another hand signal as a comparison condition. This way, everything would be the same—holding still, watching the handler and even the handler’s movements. We would vary the meaning of the signals.
“How about another hand signal,” I suggested, “which means something else?”
“Like what?” Andrew asked.
“A different type of food,” I said. “Something the dogs don’t like as much as hot dogs.”
“Like what?” Lisa asked. “Sheriff likes everything.”
It was a fine line. We wouldn’t want the dogs to eat something nasty. We needed something that they would eat but not like as much as hot dogs. Dogs are mostly carnivores. It seemed logical that they wouldn’t value a vegetable as much as a piece of meat.
“How about peas?”
Everyone nodded as they envisioned how this would work. I held up my left hand in a “stop” gesture.
“Suppose this means ‘hot dog.’ ” I thought briefly about holding up my right hand for “pea,” but as we didn’t know the extent to which dogs distinguished left and right, this seemed like a bad idea. Instead, I held both hands flat in front of my chest, pointing toward each other. “And suppose this means ‘pea’?”
Mark nodded.
“Those signals should be easily distinguishable to a dog.”
The rest of the team agreed.
It was decided. The first canine fMRI experiment would be “Peas versus Hot Dogs.”
Over the next week, Andrew and I formalized the design of the experiment, which is in some ways like writing a screenplay. Every detail has to be planned in advance. The lab walls became our storyboard. We needed to decide how many times we would give peas and hot dogs and the order of their presentation. Dogs are very good at learning sequences of things, so we wouldn’t want to simply alternate between peas and hot dogs. If we did, the dogs would know that as soon as they got a pea, the hot dog would be coming next, and there would be no need to pay attention to the hand signals. To prevent this, the order would have to be random.
The most important detail, though, would be the timing of the experiment. Each repetition would have four elements. First, the dog would place her head in the chin rest. Because of the associated movement, this would cause artifacts on the scan being acquired at that moment. We would need to wait at least two seconds for the next scan to begin. Once the dog was settled in the chin rest and enough time had passed for the artifacts to decay, we would proceed to the second element, the hand signal.
Melissa and I would be giving the signals to our dogs, and all of our attention would be focused on Callie and McKenzie. It would be too much for us to randomly decide on the fly which hand signal to give, so Andrew would be standing next to us with a pregenerated list of the order of signals. He would hold up one finger for hot dogs and two for peas. The handler, facing the dog in the scanner, would then give the corresponding hand signal. Timing was critical.
We knew that the fMRI response would not be instantaneous. The blood vessels surrounding the neurons take a few seconds to dilate, peaking after six seconds and returning to baseline twenty seconds after that. This profile is called the hemodynamic response function, or HRF, and it is a bugaboo of fMRI experiments. The lag in response meant that the dogs would have to hold perfectly still for the time it took the HRF to peak and decay. This delay period was the third element. Ideally, the dog would hold still for twenty seconds. But I would settle for ten, which would be enough time to capture at least the peak of the HRF.
Mark and Andrew and I debated whether we should just flash the hand signal for a second and then wait ten seconds before giving the reward. The alternative would be to hold up the hand signal for the entire waiting pe
riod. In the end, we opted for the latter. If we flashed the signal briefly, we wouldn’t know whether the dogs were paying attention to the appearance of the hand signal or its removal. Both could be salient. To make sure that they paid attention to the signal’s appearance, it seemed prudent to keep our hands up until we gave them the treat, which was the fourth element and the end of each sequence.
This would be easy for the hot dog repetitions. Left hand up for the signal, and then deliver the hot dog with the right hand. The pea repetitions, though, required both hands as part of the signal. This meant that the pea would have to be palmed in the right hand.
To make sure we were smooth on scan day, Melissa and I practiced all the elements over and over again. The dogs might pick up subtle changes in our body language, but there wasn’t much we could do about it other than practice.
At home, Callie and I continued working with the mockup. She was so used to it, even with the scanner noise at 95 decibels, that she was starting to get bored with the routine. She liked the hot dogs, but once inside the head coil, it was all business. No tail wagging anymore. Just a look that said, I’m here waiting for my treats. The day before scan day, we practiced for barely ten minutes. No sense in wearing her out.
Callie was ready. If she knew what was about to happen, she gave no sign.
I, on the other hand, could barely contain myself. We had made a lot of progress since the dress rehearsal. The redesign of the chin rest, the modification of the scan parameters, and the choreography of the experiment were all positive developments. But still, there was a lot riding on this. Tomorrow, we would know for sure whether the Dog Project would work.
Helen had been eagerly waiting for Dog Day too. She had made an earnest attempt to improve her study habits, making flash cards and going through them diligently. The night before scan day, I kissed her good night.
How Dogs Love Us: A Neuroscientist and His Adopted Dog Decode the Canine Brain Page 12