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.

The Monkey and the Snake

Last week’s post detailed evidence that two marine species, lemon sharks and damselfish, can learn socially, and also demonstrated that social learning can be used both to obtain food and avoid predators. In this post, I’d like to expand more on the latter, since a series of interesting research has been done on predator avoidance (or, more accurately in this case, predator fear) in monkeys.

237px-Rhesus_Macaques_-_croppedIt all began with a study by Joslin, Fletcher, & Emlen (1964) that compared the fear responses of wild-reared and lab-reared rhesus macaque monkeys to snakes. Presumably the wild-reared monkeys would have had previous experience with snakes, but the lab-reared monkeys would not. They found that only the wild-reared monkeys had a fear response to the snakes, indicating that the fear of snakes in rhesus monkeys is learned, rather than innate.

 

Cook & Mineka (and colleagues) picked up and greatly extended this line of research in the 1980s. They were interested in seeing whether this fear could be socially learned, so they exposed wild-reared monkeys to snakes while lab-reared monkeys watched. (Don’t worry – the snakes were behind plexiglass!) The lab-reared monkeys initially didn’t have a fear response to snakes, but after observing the responses of wild-reared monkeys to snakes, they exhibited a fear response. The lab-reared monkeys had socially learned to be afraid of snakes.

Interestingly, the degree of the fear response of the lab-reared monkeys was correlated with the degree of the fear response of the wild-reared demonstrator monkey observed. The greater the fear response of the demonstrator monkey, the greater the fear response of the monkey that observed him.  This indicates just how powerful social learning can be, if even the degree of the response can be transmitted!

320px-Banded_water_snake_in_AlabamaCook & Mineka next wanted to investigate whether extensive neutral prior experiences with snakes could affect whether lab-reared monkeys learned the fear of snakes. In the “immunization” condition, lab-reared monkeys observed the non-fearful responses of other lab-reared monkeys to snakes. In the “latent inhibition” condition, lab-reared monkeys were exposed to snakes for a long period of time (again, the snakes were behind plexiglass). Then both groups observed the responses of fearful monkeys to snakes. The monkeys in the latent inhibition group showed a fear response when exposed to snakes again. The immunization group, however, generally did not show a fear response to snakes (only 2 out of the 8 monkeys in this condition showed a fear response). This showed that while monkeys can socially learn to fear snakes, their initial lack of fear can also be reinforced by the non-fearful responses of other monkeys.

So far, these results agree with what we’ve already learned about social learning. But here’s where things get interesting. As I’ve mentioned before, we often study animal cognition with a view to learning more about human cognition. Cook & Mineka were interested in connecting their work on fear in monkeys to fear in humans, and specifically the very specific, intense fears we call phobias. They noted that most phobias are of things that have existed for thousands of years (like heights and, yes, snakes). However, there aren’t any phobias of more recently invented dangers (like guns). This suggests that there may be a role of evolution in the development of phobias.

In this vein, Cook & Mineka wondered if fear of anything (whether dangerous or not) could be socially learned, or if, similar to phobias, the monkeys were evolutionally predisposed to fear only certain things.

284px-Macaque_India_4To investigate this, the researchers tried to teach monkeys to be afraid of flowers. This required a little movie magic: instead of having naïve monkeys observe the responses of actual fearful monkeys, they showed them a video of a monkey reacting fearfully to a stimulus. (The researchers first verified that watching the video was just as effective at socially teaching fear as watching the actual fearful monkey.) By using video, they could manipulate the demonstrator’s response so it looked like the monkey was responding fearfully to a flower (when, in reality, it was responding fearfully to a snake). The researcher showed one group of monkeys a video of a monkey responding fearfully to a flower but not to a snake, and showed the other group a video of a monkey responding fearfully to a snake but not a flower (importantly, the responses of the monkey in the videos were exactly the same – the only difference was what it was responding to).

They found that the monkeys in the latter group, which saw the monkey respond fearfully to the snake but not the flower, developed a fear of snakes (as we would expect). However, the other group, which saw the monkey respond fearfully to the flower but not the snake, did not develop a fear of flowers or snakes. This experiment was repeated using a toy crocodile in place of a snake and a stuffed rabbit in place of a flower, with the same results. These results indicate that monkeys are evolutionally predisposed to fear certain things, but not others. They further suggest that only those fears that monkeys are predisposed to can be learned socially.

Cook & Mineka suggest a couple mechanisms for how this predisposition could work. It could be that monkeys have evolved a predisposition to fear very specific things: they have the general concept of a snake somehow stored in their brains and passed down through genes that predisposes them to fear snakes specifically. On the other hand, they could just have an instinctual knowledge of the features that make things dangerous, like sharp teeth (remember the Halloween mask study?)

320px-Coast_Garter_SnakeInterestingly, there is actually a theory (called the Snake Detection Theory) that suggests that the complex visual systems of primates developed for the purpose of detecting snakes so as to avoid them. (It also suggests that pointing developed in order to allow us to warn others about snakes.)

 

Also, in a fascinating connection to neuroscience, researchers recently discovered neurons in the pulvinar area of the brain (involved in redirection of attention and motor responses to threats) that respond quicker and more strongly to images of snakes than images of monkeys or geometric shapes. What might this result suggest about the mechanism for a predisposition to fear snakes?

Sources Cited:

Cook, Michael, and Susan Mineka. “Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys.” Journal of Abnormal Psychology 98.4 (1989): 448.

Cook, Michael, and Susan Mineka. “Selective associations in the observational conditioning of fear in rhesus monkeys.” Journal of Experimental Psychology: Animal Behavior Processes 16.4 (1990): 372.

Cook, Michael, et al. “Observational conditioning of snake fear in unrelated rhesus monkeys.” Journal of abnormal psychology 94.4 (1985): 591

Isbell, Lynne A. The fruit, the tree, and the serpent: why we see so well. Harvard University Press, 2009.

Joslin, J., H. Fletcher, and J. Emlen. “A comparison of the responses to snakes of lab-and wild-reared rhesus monkeys.” Animal Behaviour 12.2 (1964): 348-352.

Mineka, Susan, et al. “Observational conditioning of snake fear in rhesus monkeys.” Journal of abnormal psychology 93.4 (1984): 355.

Mineka, Susan, Richard Keir, and Veda Price. “Fear of snakes in wild-and laboratory-reared rhesus monkeys (Macaca mulatta).” Animal Learning & Behavior 8.4 (1980): 653-663.

Mineka, Susan, and Michael Cook. “Immunization against the observational conditioning of snake fear in rhesus monkeys.” Journal of Abnormal Psychology 95.4 (1986): 307.

Van Le, Quan, et al. “Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes.” Proceedings of the National Academy of Sciences 110.47 (2013): 19000-19005.

Just Keep Learning, Just Keep Learning…

Last week we discussed how horses are able to learn from other horses to access hidden food. This week, I’d like to talk about whether very different animals can also utilize social learning: sharks and fish.

320px-Lemon_shark2I’ve never thought of sharks as social animals, so it surprised me that someone would investigate whether sharks can socially learn. However, while many shark species are solitary, some species do live in groups. Guttridge et al. (2013) studied the ability of one such species, the lemon shark, to learn from other lemon sharks.

They taught one group of lemon sharks (the “demonstrators”) to approach an underwater target, then rewarded them with food. Once the sharks had learned this association, one demonstrator was paired with a naïve “observer” shark and completed five trials. Then the demonstrator was removed and the observer was tested alone.

Guttridge et al. also had a control group of “sham” demonstrators, which had not been trained on the task. These sharks were also paired with naïve observers, exposed to five trials of the task, and removed. Then the “sham” observers were tested. The performance of the observers was compared to that of the sham observers to rule out the possibility that the observers’ behavior was due to merely being in the presence of another shark.

The researchers found that the observers completed more trials than the sham observers. Additionally, the observers were much faster to complete their very first trial than the sham observers, although the sham observers quickly learned the task from experiencing it themselves. Even though the sham observers caught up to the observers in performance, the fact that the observers were quicker on the first trial indicates that social learning did occur.

At its most basic level, social learning means learning about one’s environment from a more experienced individual. We’ve seen how social learning can be used for the purpose of obtaining food in an animal’s environment. Can social learning be used to avoid dangers in an environment as well?

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Tropical Damselfish (A. polyacanthus)

Manassa & McCormick (2012) investigated this question in tropical damselfish. The researchers wanted to see if damselfish could learn to recognize a predator solely based the behavior of another damselfish. Recognition of a predator was indicated by an “anti-predator response”: remaining close to shelter (in this case, a rock in the tank).

First the researchers made sure that the damselfish didn’t initially recognize a particular predator fish’s odor by pouring 60 mL of water from the predator fish’s tank into the damselfish tanks, and observing the damselfishes’ responses. The damselfish showed no anti-predator response, confirming that they didn’t instinctively recognize the predator fish.

Next the researchers conditioned a group of damselfish to recognize the predator. To do this, they utilized an interesting trait of damselfish (and some other fish species): the fish release a chemical alarm signal when injured, which warns nearby conspecifics (members of the same species) of a possible threat. Manassa & McCormick added predator odor to the tanks of “demonstrator” damselfish, followed by damselfish chemical alarm signal. They later tested these damselfish by adding just predator odor to their tanks. The demonstrators exhibited an anti-predator response, remaining close to shelter, proving that they now recognized the predator fish.

ChocHind

Predator Fish: Chocolate Hind (C. boenak)

In the next stage, demonstrators were paired with naïve damselfish and predator odor was once again added to the tank. Finally, the demonstrator was removed, predator odor was added a final time, and the behavior of the previously naïve (now “conditioned”) damselfish was observed.

Manassa & McCormick found that, compared to control damselfish that had been paired with other naïve damselfish, the conditioned damselfish moved closer to shelter in response to the predator odor. In fact, their response was no different from the response of the demonstrator damselfish that had been trained with both predator odor and the chemical alarm signal. These results indicate that tropical damselfish can socially learn about predators.

So it turns out that animals across the animal kingdom can utilize social learning to learn about their environments and increase their chances of survival. Next week we’ll finish up talking about social learning with an example of social learning interacting with genes!

Here’s a cool video detailing a few other social learning experiments in fish. (The title, “Culture in Fish”, may seem a bit surprising, as we don’t usually think of animals as having culture. It’s still a controversial idea in the fields of animal behavior and cognition, and I’m hoping to go into more detail in a future post. But suffice it to say that many scientists contend that social learning is closely tied to culture.)

Sources Cited:

Guttridge, Tristan L., et al. “Social learning in juvenile lemon sharks, Negaprion brevirostris.” Animal cognition 16.1 (2013): 55-64.

Manassa, R. P., and M. I. McCormick. “Social learning and acquired recognition of a predator by a marine fish.” Animal cognition 15.4 (2012): 559-565.

Learning from a “Neigh”bor

They say that the best way to learn how to do something is to do it yourself. I don’t know about you, but I much prefer the somewhat lazier option of learning how to do something by watching others do it. This method, known as social learning, involves more complex cognitive processes (figuring out what the other individual is doing, and understanding that you can use the same method to achieve the same result) than individual learning. But it also has some advantages, chiefly the ability to learn without directly experiencing any of the accompanying dangers or consequences.

It’s no surprise, then, that many animals are able to utilize social learning. I’d love to discuss the wide range of animals that use social learning in a future post, but today I’m going to focus on a single study done on social learning in horses. This study is particularly interesting because it also investigates some factors that influence whether a horse learns socially or not.

303px-Arizona_2004_MustangsKrueger et al. (2013) investigated whether horses could learn to access hidden food just by watching other horses. First, they trained some horses to open a food-filled drawer by pulling on a rope; these horses then became demonstrators for the rest of the horses (the “observers”).

In each trial, an observer horse watched a demonstrator open the drawer and eat the food. Then the demonstrator was led away, the drawer was refilled with food and closed, and the observer was allowed to approach the drawer. Once the observer consistently opened the drawer after the demonstrator, she was tested without the demonstrator.

A third group of horses participated in a control experiment, where they were given access to the closed drawer without training or demonstrations. The success rate of these control horses was compared to that of the observers to determine whether seeing the demonstrators open the drawer led to a higher success rate (i.e. social learning occurred).

4598811547_1d257e2c9e_m12 of the 25 observer horses learned to open the drawer, whereas only 2 of the 14 control horses did, showing that horses can use social learning to find hidden food. But perhaps the most interesting result comes from comparing the 12 observers who learned to the 13 who didn’t. Krueger et al. found that the “learner” horses were younger, ranked lower in the group’s social hierarchy, and more exploratory than the “non-learner” horses. (The researchers measured how exploratory the horses were by seeing how much they touched novel objects that were presented to them.)

Krueger et al. took a closer look at the relationships between age, social rank, amount of exploration, and social learning. They found that the younger the horse, the faster it learned. No such relationship was found with social rank and amount of exploration. This, along with other analyses, suggests that age has the biggest influence on whether a horse socially learns or not.

The researchers hypothesize that older horses could be less able to socially learn simply due to their age. Additionally, although social learning is most often beneficial to the learner, it can also result in learning behavior that is disadvantageous. Older horses could be less willing to learn socially in order to minimize this risk. This could be enhanced by the fact that the demonstrators in this experiment were younger than the older, non-learning horses. Older horses could generally not learn behavior from younger horses because, due to their lack of experience, younger horses may engage in more dangerous or risky behaviors.

468273357_0ac370df68_nThis experiment showed that horses are able to learn socially, although more research needs to be done on the factors influencing social learning on an individual level. Besides those discussed here, what factors do you think would affect whether an animal can (or chooses to) socially learn?

Next week we’ll look at social learning in a very different group of animals (think water…)!

Source Cited:

Krueger, Konstanze, Kate Farmer, and Jürgen Heinze. “The effects of age, rank and neophobia on social learning in horses.” Animal cognition (2013): 1-11.