fMRI in Dogs

We can learn a lot about animal cognition by using behavioral experiments, where we rely on the actions of an animal in a particular situation to infer what processes are occurring in the animal’s brain. But what about looking more directly at what the brain is doing?

One way to do that is to record the activity of neurons in the brain using electrodes. There are a few downsides to this method, though. First, neural recordings can only show us the activity of very small areas of the brain at a time. Additionally, the animals used in these experiments have usually been raised in a lab, rather than in their natural environment, which could affect their cognitive development.

263px-MRI-Philips

MRI Machine

Another way to look at brain activity is through imaging such as functional Magnetic Resonance Imaging, or fMRI. The MRI machine uses a magnetic field to look at oxygen flow to different areas of the brain. More active brain areas need more oxygen, so by tracking the oxygen flow to the brain over time, we can determine the pattern of activity in the brain. And, unlike with neural recordings with electrodes, we can look at the activity of the entire brain at once.

 

Unfortunately, fMRI requires that the person (or animal) being scanned lie completely still inside the MRI scanner, which is a bit confining and noisy. While this isn’t a problem for anesthetized animals, it’s nearly impossible for awake animals. But recently, researchers have made incredible progress in using fMRI to study dogs.

In 2012, a group of researchers managed to train two dogs to lie still in an MRI machine long enough to have their brains scanned. They first got the dogs used to laying with their chins in a chin rest, then slowly acclimated them to the noise of the machine, ear muffs (to muffle some of the machine’s noise), and the MRI machine itself. While in the scanner, the dogs were shown two different hand signals: one was followed by a food reward (“reward”), while the other was not (“no reward”).

The researchers were interested in the response of an area of the brain called the caudate nucleus. Among other important functions including voluntary movement and learning, the caudate nucleus in involved in the reward system of the brain; previous studies have found that the caudate becomes more active when a reward is expected.

2241616932_107199f0fa_mSure enough, the researchers found that the dogs’ caudate nuclei were more active when the “reward” hand signal was given than when the “no reward” signal was given. They later replicated this study with 11 more dogs and found that the increase in activity in the caudate was comparable to that found in humans. Interestingly, some of the dogs studied were service dogs, and they had nearly significantly greater caudate activation than the non-service dogs when the “reward” hand signal was given. The researchers theorized that, due to their extensive training, the service dogs may have found the hand signal itself intrinsically more rewarding.

(Check out the Supporting Information for the first paper for an interesting video detailing the training that the dogs underwent!)

Before these studies, fMRI studies with animals required that they be restrained or anesthetized, both of which could greatly affect brain activity. Believe it or not, researchers actually ran studies investigating brain activity in response to odors…in anesthetized dogs! While the brain does respond to such stimuli even under the influence of anesthesia, it clearly does so in a different way than it would normally. (Of course researchers were aware of this, but there just wasn’t another option at the time.)

Once it had been shown that dogs could be trained to lie still in an MRI machine, some researchers decided to see just how different the brain’s response to odors is in anesthetized and awake dogs. They found that, in addition to the sensory brain areas active in anesthetized dogs, the frontal cortex was activated by odor in awake dogs. (The frontal cortex is implicated in complex cognitive functions like decision-making and planning.) The researchers suggested that the frontal cortex activity could be involved in understanding what an odor means in a particular context, and could inform how the dog behaves in response to that odor. Understanding this kind of brain activity could have major implications for how we train drug- and bomb-sniffing dogs.

443627085_4fe6f95f01_mThe first group of researchers also studied dogs’ brain activity in response to odors. They presented dogs with five different odors: a familiar dog, an unfamiliar dog, the dog itself, a familiar human, and an unfamiliar human. They found that, compared to the other four odors, there was greater activity in the caudate nucleus in response to the familiar human odor. This indicates that not only could the dogs discriminate between the different odors, but that they also associated that particular human with reward. And again, the researchers found that the response was stronger in service dogs, possibly due to their more extensive human contact during training.

Finally, another group of researchers compared the brain activity of humans and dogs as they were listening to human and dog vocalizations and natural sounds. They found that similar areas of the brain were more active when they heard the vocalizations of conspecifics (i.e. when humans heard humans and dogs heard dogs). This suggests that these brain areas may have evolved for that particular purpose more than 30 million years ago (although convergent evolution is a possibility). Additionally, some brain areas responded more strongly to more positive vocalizations (i.e. laughing versus crying). These brain areas were in similar locations in both dogs and humans, and responded to both species’ vocalizations. This suggests that dogs and humans may have comparable emotional processing of sounds.

Interestingly, part of the training of the dogs used in this study involved social learning – naïve dogs watched an experienced dog get in the MRI scanner and receive praise and treats, which motivated the naïve dogs to behave in the same way!

(Although the paper of this study isn’t freely available, the researchers did make a fascinating video summarizing their study, and NPR wrote an article about it.)

4840054871_b79aef16f2_mStudying canine cognition using fMRI is a relatively new application of the method, but the research so far looks promising. Not only will it allow us to get a direct look at what’s going on in dogs’ brains, but it could also improve the way we train service dogs and care for our best friends.

 

I’ll end with a thought-provoking quote from one of the above papers, about canine cognition research:

“…While the study of the canine mind is fascinating for its own sake, it also provides a unique mirror into the human mind. Because humans, in effect, created dogs through domestication, the canine mind reflects back to us how we see ourselves through the eyes, ears, and noses of another species.”

-Berns et al. (2012)

 

Sources Cited:

Andics, Attila, et al. “Voice-Sensitive Regions in the Dog and Human Brain Are Revealed by Comparative fMRI.” Current Biology (2014).

Berns, Gregory S., Andrew M. Brooks, and Mark Spivak. “Functional MRI in awake unrestrained dogs.” PloS one 7.5 (2012): e38027.

Berns, Gregory S., Andrew Brooks, and Mark Spivak. “Replicability and Heterogeneity of Awake Unrestrained Canine fMRI Responses.” PloS one 8.12 (2013): e81698.

Berns, Gregory S., Andrew M. Brooks, and Mark Spivak. “Scent of the Familiar: An fMRI Study of Canine Brain Responses to Familiar and Unfamiliar Human and Dog Odors.” Behavioural Processes (2014).

Jia, Hao, et al. “Functional MRI of the Olfactory System in Conscious Dogs.” PloS one 9.1 (2014): e86362.

Creatures of Habit

We’ve all been in situations that seem too good to be true: something unexpectedly good happens, and instead of just enjoying it, we pause, looking for the trick or catch.

Whats_for_dinnerIt turns out monkeys may do this as well. Knight et al. (2013) taught macaque monkeys to accept (or reject) offered treats by pushing (or not pushing) a button. First, a researcher would show the monkey the treat to be offered (a pellet or mini marshmallow), then take it away. The button would then light up, indicating to the monkey that the official offer was forthcoming. Finally, the monkey was presented with the treat again. If he pushed the button, “accepting” the offer, then he would receive the treat. (Unsurprisingly, the monkeys never “rejected” any of the offered treats. But the researchers wanted to make sure the option was available.)

After the monkeys learned the task, the researchers changed it up a bit to see how they would react. Instead of offering the same treat that was first presented, the researchers offered a different treat. So on some trials, the monkeys were offered an unexpectedly worse treat (presented with a mini marshmallow but offered a pellet), while on others, they were offered an unexpectedly better treat (presented with a pellet but offered a mini marshmallow).

On the worse-than-expected trials, the monkeys still accepted all of the offers, but their latencies to accept (i.e. push the button) were significantly longer than when they were offered the same treat that was presented to them. This result agrees with a previous study where macaques exhibited confusion and negative reactions when they found an unexpected less-desired food instead of the expected more-desired food hidden under a cup. And it makes evolutionary sense for animals to desire the outcome (in this case, food) that has a greater value to them.

Based on this logic, we might expect the monkeys to accept the better-than-expected offers faster than the worse-than-expected offers (and possibly even the expected offers). However, the latencies to accept the better-than-expected offers were actually more than twice as long as the worse-than-expected offers. Moreover, the monkeys exhibited significantly more negative responses, frequently avoiding looking at the mini marshmallows by averting their eyes or head (a type of behavior often seen in fear tests).

We know from previous research that animals behave in a way to maximize the value of outcomes (for example, getting the best possible food), so why would the macaques respond negatively to receiving a better-than-expected treat?

8774415224_ac7e9deb0e_mBecause of another important principle that guides our actions: consistency. Animals, including humans, love routine and consistency. And with good evolutionary reason, as the unexpected can often be dangerous. We therefore like to be able to make accurate predictions about our world, and generally aren’t happy when our expectations are wrong.

So in this case, the simple inconsistency between expectation (presented treat) and outcome (offered treat) could have caused the longer acceptance latencies, regardless of the direction of the outcome (better or worse).

But why were the macaques’ reactions to better-than-expected offers even more negative than those to worse-than-expected offers? The researchers suggest that the macaques may also have a sort of “too good to be true” mentality. After all, unexpected outcomes are much more likely to be negative than to be positive. (If you go to the same banana tree every day, you’re more likely to find fewer bananas and more predators than you are to find an unexpected overabundance of bananas and zero predators.) The monkeys who survive to pass on their genes are the ones who assume all surprising outcomes are bad, and respond cautiously to seemingly good surprising outcomes, just in case.

It seems that, at least in this study, the principle of consistency takes precedence over the principle of maximizing outcome value. This result can give us insight into the kinds of considerations primates take into account when making decisions. Based on the results of this study, if a monkey had to choose between an action with a less predictable but potentially greater outcome value, or an action with a more predictable but smaller outcome value, which action might it choose?

 

Sources Cited:

Knight, Emily J., Kristen M. Klepac, and Jerald D. Kralik. “Too Good to Be True: Rhesus Monkeys React Negatively to Better-than-Expected Offers.” PloS one 8.10 (2013): e75768.

Tinklepaugh, Otto Leif. “An experimental study of representative factors in monkeys.” Journal of Comparative Psychology 8.3 (1928): 197.