Laughing It Up

320px-Fancy_rat_blazeIn skimming journals to find articles to discuss on this blog, I frequently see studies that, based on title alone, seem a bit unbelievable. Recently I came across the most unbelievable-sounding one so far: Laughing Rats are Optimistic. Rats can be optimistic? How would you even measure that? Wait – rats can laugh?


To begin with the last question, yes, actually, they can. Rats make certain Ultrasonic Vocalizations (USVs) – sounds that are too high-pitched for humans to hear – that seem to be analogous to human laughter. For example, rats emit these USVs in response to pleasant stimuli, and when playing or being tickled. Additionally, stimulating the reward circuit of the brain increases the rates of USVs in rats.

If these USVs are truly analogous to human laughter, then they similarly serve as an indicator of a positive affective state in rats. Put more plainly, these USVs are a sign that a rat is happy. And this could be good information to know because, in humans, emotional state can greatly affect cognitive processes like decision-making. What if the same is true for animals?

Rygula et al. (2012) wanted to know if rats in a positive affective state are also more optimistic. We know how to tell us if a rat is in a positive affective state (USVs), and also how to put a rat in a positive affective state (tickling). But how can we tell if a rat is optimistic?

The researchers began by teaching the rats a very simple task. If a particular (“positive”) tone was played, the rat could push one lever (the “positive” lever) to receive a reward. If a different (“negative”) tone was played, the rat had to push another lever (the “negative” lever) to avoid a punishment (a small shock to the foot). The rats easily learned these associations, and were able to discriminate between the two tones.

WT_and_TK_rat_photoBut how would the rat respond if the researchers played a tone in between the positive and negative tones? An optimistic rat would expect the tone to indicate a reward, so it would be more likely to push the positive lever. A pessimistic rat, on the other hand, would expect the tone to indicate a punishment, so it would be more likely to push the negative lever.

After training the rats on the initial task, Rygula et al. tested the rats on the intermediate tone in two different sessions. In one session, the rats were tickled before being tested; in the other session, they were merely held before being tested.

Overall, the rats didn’t push the positive lever significantly more often after being tickled than after being held. However, when they took a closer look at the data, the researchers found individual differences in how much the rats laughed in response to the tickling; some rats laughed a lot, while others barely laughed at all. The researchers thus divided the rats into two groups (those that laughed when tickled and those that did not) and analyzed the data again. They found that the rats that laughed when tickled did press the positive lever significantly more often after being tickled than after being held. There was no significant difference found for the rats that didn’t laugh when tickled.

These results indicate that laughing rats are indeed more optimistic, and more generally, that affect can influence cognitive processes like decision-making in rats. This study also serves as an important reminder to be aware of individual differences in subjects; although it had been previously shown that tickling could elicit USVs, it clearly didn’t do so for all rats (or at least not to the same degree). By just combining the results of all the rats, the significant relationship between USVs and optimism was obscured.


Here’s a short video about detecting rat laughter (and how to tickle a rat). In addition to rats, non-human primates and dogs also laugh. In fact, it’s been found that playing recordings of dog laughter for shelter dogs actually decreases their stress behaviors!


Source Cited:

Rygula, Rafal, Helena Pluta, and Piotr Popik. “Laughing rats are optimistic.” PloS one 7.12 (2012): e51959.

Planning Ahead

Planning for the future is one of our most important – and complex – cognitive abilities. It requires the ability to make predictions about future events or states by relying on knowledge and past experiences. More basically, it requires us to disconnect ourselves from our current state, including our current emotions and motivations, to anticipate our future emotions and motivations. Scientists call this ability “mental time travel”, or chronesthesia.

As with many cognitive abilities discussed here, the mental time travel ability was initially thought to belong only to humans (the Bischof-Köhler hypothesis). However, an ingenious study done with scrub jays has demonstrated that animals may possess this ability, too.

Scrub jays, which belong to the same family as crows and magpies, cache excess food, hiding it in various places that they can access when food is scarce. This behavior may seem like planning ahead, but it could just be an automatic response to an abundance of food or the season.

Raby et al. (2007) investigated whether scrub jays could demonstrate planning for the future in a very specific way through their caching behavior. Each jay was housed in a cage divided into three compartments. The jay was fed every evening in the middle compartment. Each of the side compartments contained a caching tray, where the jay could hide food. During the day, the jay could move freely between all of the compartments. However, each morning, the jay was restricted to one of the two side compartments for two hours. In one compartment, the jay was always fed a breakfast of (uncachable) powdered pine nuts. In the other compartment, the jay was never fed breakfast, and had to wait two hours for food.

During a training phase, each jay spent a few mornings in each of the side compartments, in order to learn the associations between one compartment and breakfast, and the other compartment and no breakfast. The jay was only fed powdered pine nuts, so no caching occurred during the training phase.

After the training phase came the critical test: when given whole pine nuts (which can be cached) in the evening, would the jay cache more nuts in the no-breakfast compartment than the breakfast compartment? Such behavior would indicate that the jay was planning for the future by caching more food where it knew food would be scarce. However, if the jay cached similar amounts of nuts in both of the side compartments, then it was not planning for the future.

Raby et al. found that the jays cached significantly more nuts in the no-breakfast compartment than in the breakfast compartment, indicating that they were planning ahead. This is especially impressive because it required the jays to take into account both their future motivational state (i.e. hunger) and future available resources (breakfast or no breakfast), and suggests that they have the ability of mental time travel.

In addition to planning for the future, mental time travel also includes remembering past events (episodic memory). There’s even evidence that these cognitive processes (planning for or imagining the future and remembering or imagining the past) involve similar areas of the brain in humans!

For a more thorough discussion of mental time travel and whether non-human animals have this ability, check out this paper.


Source Cited:

Raby, Caroline R., et al. “Planning for the future by western scrub-jays.” Nature 445.7130 (2007): 919-921.

Look Who’s Talking

Although they don’t have language the way humans do, animals can clearly communicate with each other (otherwise, why would they make sounds at all?). We usually view animals’ vocalizations as reflexive (a yelp in response to pain) or very general (a threatening growl), but research in the past few decades has shown that animal vocalizations can be remarkably specific.

320px-Präriehund_P1010308Some of the most specific communication has been found in the alarm calls of prairie dogs. Prairie dogs live in burrows in the ground, making them vulnerable to predators, so it’s very important for them to be able to communicate the presence of a predator to the rest of the colony. Moreover, because different predators have different attack strategies (a hawk would attack from the air, whereas a dog would attack from land), it’s also important for prairie dogs to communicate what kind of predator is nearby so the most appropriate escape response can be made.

Researchers have found that prairie dogs do indeed make different alarm calls depending on the species of predator spotted. However, just because a prairie dog makes a predator-specific alarm call doesn’t mean that other prairie dogs interpret it as such; it’s possible that prairie dogs can make distinctions between predators when giving alarm calls yet not respond to these distinctions when hearing other prairie dogs’ alarm calls. They could rely on other cues, such as the behavior of the prairie dog that made the alarm call or the predator itself, to make the appropriate escape response.

In order to test whether prairie dogs can distinguish between different types of predator calls, researchers ran a playback experiment. First researchers recorded alarm calls made by prairie dogs in response to seeing different types of predators. They later played back these calls in the absence of a predator and looked at the prairie dogs’ responses.

4838957259_c0a458c8ba_mIf the prairie dogs truly understand that different types of calls are associated with different types of predators, then they will respond appropriately based on the predator. The researchers found that the prairie dogs did just this. When they heard an alarm call to a hawk, they immediately ran into their burrows, the typical response to a hawk predator. When they heard an alarm call to a dog, they became alert but didn’t immediately enter their burrows, just as they would respond to the presence of a dog.

These results demonstrate something very important about prairie dog alarm calls: these calls are referential, meaning that they refer to an object (or in this case, animal), rather than being reflexive. This is significant because, until the last few decades or so, it was thought that the referential nature of human language was one of the characteristics that set it apart from other animal communication.

240px-Kissing_Prairie_dog_edit_3Further research on prairie dog alarm calls has shown just how specific they can be. Multiple studies have shown that prairie dogs have different alarm calls for different humans, and for the same human wearing different colored shirts, suggesting that prairie dogs can encode color and shape information into their calls. Researchers have also found regional differences between calls, where the acoustic differences between calls for the same predator are greater between colonies that are geographically farther away.

And prairie dogs aren’t the only species with specific vocalizations: vervet monkeys, Diana monkeys, Campbell’s monkeys, ground squirrels, and chickens (to name just a few) have all demonstrated different alarm calls for different types of predators.

So if these vocalizations are so specific and referential, do they count as language? It’s definitely a contested issue (as you would expect). Few scientists would argue that these vocalizations are the same type of language as that of humans. However, these vocalizations suggest that the cognitive structures involved in human language may have evolved earlier than we previously thought. And they’ve certainly made scientists rethink what exactly a “language” is!


Here’s an interesting video about prairie dog alarm calls by Con Slobodchikoff, who has done nearly all of the research out there on prairie dog vocalizations. And here’s a video with Robert Seyfarth (who, along with Dorothy Cheney, has done an incredible amount of research on vervet vocalizations) about whether such specific vocalizations count as language. Finally, here’s a video of vervet alarm calls in action!


Sources Cited:

Ackers, Steven H., and C. N. Slobodchikoff. “Communication of stimulus size and shape in alarm calls of Gunnison’s prairie dogs, Cynomys gunnisoni.” Ethology 105.2 (1999): 149-162.

Frederiksen, J. K., and C. N. Slobodchikoff. “Referential specificity in the alarm calls of the black-tailed prairie dog.” Ethology Ecology & Evolution 19.2 (2007): 87-99.

Kiriazis, Judith, and C. N. Slobodchikoff. “Perceptual specificity in the alarm calls of Gunnison’s prairie dogs.” Behavioural processes 73.1 (2006): 29-35.

Slobodchikoff, C. N., S. H. Ackers, and M. Van Ert. “Geographic variation in alarm calls of Gunnison’s prairie dogs.” Journal of Mammalogy (1998): 1265-1272.

Slobodchikoff, C. N., and R. Coast. “Dialects in the alarm calls of prairie dogs.” Behavioral Ecology and Sociobiology 7.1 (1980): 49-53.

Slobodchikoff, C. N., C. Fischer, and J. Shapiro. “Predator-specific alarm calls of prairie dogs.” American Zoologist 26 (1986): 557.

Slobodchikoff, C. N., et al. “Semantic information distinguishing individual predators in the alarm calls of Gunnison’s prairie dogs.” Animal Behaviour 42.5 (1991): 713-719.

Slobodchikoff, C. N., Andrea Paseka, and Jennifer L. Verdolin. “Prairie dog alarm calls encode labels about predator colors.” Animal cognition 12.3 (2009): 435-439.

When Less is Worth More

Often when problem solving, we don’t have the time or cognitive capacity to painstakingly evaluate each solution. Instead, we make an educated guess or rely on our common sense or a rule of thumb. These shortcuts (called “heuristics”) may save us time and cognitive processing, but they don’t always lead to the optimal solution.

Take, for example, the “less is better” effect: valuing a single, high quality object more than that same high quality object plus an object of lower quality. The addition of the lower quality object somehow decreases the subjective value of the higher quality object, even though the quantity of the two objects is greater than the high quality object alone.

286px-HFG_Hans_(nick)_Roericht-_TC100-_dish_set-dhubThis may seem ridiculous, but humans have clearly demonstrated this effect. In one experiment, Hsee (1998) asked participants to indicate how much they would be willing to pay for a set of dishes. In one condition, the set contained 24 dishes. In another condition, the set contained 40 dishes, but 9 of them were broken. Even though the second condition contained more unbroken dishes than the first, the amount that participants were willing to pay for the first set was greater than for the second set. The inclusion of some broken dishes decreased the value of the second set, even though it actually contained more unbroken dishes than the first set.

It’s important to note that participants weren’t comparing the two sets of dishes directly; each participant was only asked to name a price for one set of dishes. Their responses, then, were based on their valuation of the particular set of dishes without additional information or comparison.

When Hsee asked participants to name prices for both sets of dishes, the “less is better” effect disappeared. Instead, participants said that they would pay more for the larger set of dishes than the smaller one. This indicates that humans use comparison information (when it’s available) to make valuation judgments, and we can use this information to overrule heuristics and arrive at the optimal choice. But when we don’t have that comparison information, our heuristics can sometimes steer us wrong.

What about nonhuman animals? Do they rely on similar heuristics when problem solving, and thus make similar suboptimal choices?

Kralik et al. (2012) investigated whether rhesus macaques would also demonstrate the “less is better” effect. In both the lab and a more naturalistic setting, they gave the macaques two options: a more-preferred treat (like a grape), or a more-preferred treat AND a less-preferred treat (like cucumber).

8774415224_ac7e9deb0e_mThey found that the macaques chose the grape alone significantly more than the grape + cucumber. At first glance, this doesn’t make sense; when given the choice between more food and less food, it’s more evolutionarily advantageous to choose more food. However, it seems that the macaques were more concerned with the quality of the choice than the quantity, and somehow the presence of the less-preferred cucumber lowered the quality of the more-preferred grape. So the decision was instead between lower-quality food (grape + cucumber) and higher-quality food (grape).

It turns out that focusing on quality more than quantity might actually make evolutionary sense: research on the foraging behavior of animals suggests that, when food is scarce, focusing on the quality of food in a particular location (rather than quantity) may lead to more optimal foraging decisions (Do I keep eating at this tree or move on to another one?). Additionally, when food is abundant, averaging the quality of all the food in a particular location will maximize outcome.

So it seems that when solving this problem, macaques rely on a heuristic that may maximize outcome in the wild, even though it doesn’t maximize outcome in this particular task. And, unlike humans, macaques aren’t able to use comparison information to override the heuristic and make the optimal choice. Perhaps factoring in comparison information requires higher cognitive processes that macaques don’t possess, or perhaps macaques just need more experience with the task in order to factor in comparison information.

2802429078_ec607610f9_mEither way, the results of these experiments suggest that some heuristics may have an evolutionary origin that predates the split between humans and other primates. And they may have developed even earlier than that: Pattison & Zentall (2014) recently found that dogs also demonstrate the “less is better” effect!

If you’ve enjoyed reading about animal cognition research on this blog, check out Inside Animal Minds, a short NOVA series on animal cognition. The first episode airs tonight at 9 pm on PBS!


Sources Cited:

Hsee, Christopher K. “Less is better: When low-value options are valued more highly than high-value options.” Journal of Behavioral Decision Making 11.2 (1998): 107-121.

Kralik, Jerald D., et al. “When less is more: Evolutionary origins of the affect heuristic.” PloS one 7.10 (2012): e46240.

Pattison, Kristina F., and Thomas R. Zentall. “Suboptimal choice by dogs: when less is better than more.” Animal cognition (2014): 1-4.

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.


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.

Mirror, Mirror

1471836761_11edeb5212_mHumans use mirrors so easily that we often don’t think about the cognitive processes required to do so (although we do derive entertainment from those animals that just don’t “get” mirrors). Being able to recognize oneself in the mirror doesn’t seem like an evolutionarily advantageous skill, but scientists think that this ability may indicate the possession of other skills more relevant to survival.

For example, mirror self-recognition may be indicative of self-consciousness and, by extension, theory of mind (the ability to think about what others may be thinking); being self-conscious, or having knowledge of the self, may naturally lead to having knowledge of others. These skills are especially important for social animals, as theory of mind allows us to take the perspective of others, which is the basis for empathy. (Evidence for the connection between mirror self-recognition and theory of mind comes from studies with young children, which have found that mirror self-recognition and perspective-taking abilities develop at around the same time.)

But how can we tell whether animals and pre-linguistic children connect what they see in the mirror to their physical selves? The most commonly used measure is the Mirror Test (also called the Mark Test or the Rouge Test), which was developed by Gordon Gallup, Jr. in 1970. After a familiarization period with a mirror, a colored mark is placed on an area of an animal that can’t be seen without the use of a mirror (usually somewhere on the face). The animal is then exposed to a mirror again, and her behavior is closely monitored. If the animal touches the mark on her own face (rather than the mirror), then she has “passed” the Mirror Test and demonstrates mirror self-recognition.


Not quite there yet…

When first exposed to a mirror, most animals (including humans) exhibit social behaviors like lip smacking and attempts to play, indicating that they perceive their reflection as a conspecific. After some cognitive development and experience with mirrors, however, some animals will demonstrate mirror self-recognition (for humans, this occurs around 18-24 months of age).

Unsurprisingly, humans’ closest evolutionary relatives, the great apes, demonstrate mirror self-recognition (the great apes include chimpanzees, bonobos, gorillas, and orangutans; all have passed the Mirror Test). Additionally, some very distant relatives of humans, but who are also highly social and have demonstrated advanced cognitive abilities, have passed the Mirror Test: dolphins and elephants.

One unexpected species that has passed the Mirror Test is the magpie. But when you consider their other cognitive abilities, it’s not so surprising: magpies have also demonstrated the abilities of tool use, perspective-taking, and foresight. (Why would these abilities be particularly helpful to magpies? Researchers theorize that they enable magpies’ prolific thievery.)

7193567450_b7ebd10bb2_mInterestingly, lesser apes (gibbons) and monkeys fail the Mirror Test, suggesting that mirror self-recognition and all the attendant cognitive abilities (self-consciousness, perspective-taking, etc.) evolved after the evolutionary split between great and lesser apes (which occurred after the split between apes and monkeys). Elephants, dolphins, and magpies, then, must have evolved the abilities through convergent evolution.

So it seems pretty simple: pass the Mirror Test, and you demonstrate mirror self-recognition and its associated cognitive abilities. Yet, as with most matters in animal cognition, this one is far from cut-and-dry.

Some researchers have argued that the Mirror Test isn’t appropriate for many animals. First, a colored mark on the face may not be salient enough for some animals (it may not stand out or be important enough for the animals to notice). Additionally, just because an animal doesn’t touch or try to remove the mark doesn’t mean he doesn’t recognize his reflection; perhaps he notices the mark but just doesn’t care. Finally, what about animals who have poor vision, or who rely primarily on other senses? Surely we can’t say they lack the abilities of self-consciousness and perspective-taking simply because they don’t pass the Mirror Test.

This issue is complicated even when studying children: some studies have shown vast cultural differences in performance on the Mirror Test. For example, many of the Kenyan children in one study froze in response to seeing their reflections. While some of these cultural differences could be attributed to differences in experience with mirrors, researchers think they are likely more related to different parenting styles and differences in how the children understand the task. Children raised in cultures with a high emphasis on obedience, for example, may recognize their reflections but be unsure of whether they’re allowed to investigate or remove the mark.

1921632741_baee2c47b8_mThese criticisms of the Mirror Test have prompted some researchers to try to find other methods of gauging whether animals demonstrate mirror self-recognition. Some possible alternative indicators include mirror-guided self-directed behaviors (like using the mirror to examine one’s body) and the disappearance of social responses to the mirror. Some researchers attempted to use these indicators as proof that macaques can recognize themselves in the mirror, although their interpretation has been questioned. (I highly recommend reading these papers and judging for yourself – you can find the original paper here. Unfortunately, the rebuttal paper isn’t available for free, but the same authors briefly discuss their criticisms in this article.)

This brings me to a tangential point about scientific research in general. These kinds of exchanges regularly occur in science, regardless of the particular field. Often, one researcher (or a group of researchers) finds an issue with another researcher’s methods or conclusions. Sometimes she will just write a rebuttal pointing out the flaws she sees or offering an alternate interpretation of the results, but she may also conduct her own experiment, fixing any methodological flaws from the original study. While it is undoubtedly frustrating to have your methods and conclusions questioned, it ultimately leads to better science by pushing researchers to really think about and improve task design and to be very careful about interpreting results.

It is also the theoretical basis of how we disseminate findings in the scientific community: after careful consideration by other scientists in the field (peer review), we publish not only the conclusions of our experiments, but also our exact methods, our data, and the related prior research that helps lead us to those conclusions. In essence, we tell a story about our research. Others can then follow along and, rather than taking our word for it, decide for themselves whether our story is compelling and what makes it so (or not).

(As I said, though, this is all in theory. There is currently quite a bit of debate concerning how papers are chosen for journals, whether access to these papers should be free to everyone, and a host of other issues relating to publishing scientific research.)

174px-Mirror_test_with_a_BaboonBut I digress. Hopefully this was a thought-provoking summary of what mirror self-recognition can (but possibly can’t) tell us about certain cognitive abilities. I’ll leave you with this video about the Mirror Test in primates (starts at 1:00), and this one about dolphins and elephants.





Anderson, James R., and Gordon G. Gallup. “Do rhesus monkeys recognize themselves in mirrors?.” American journal of primatology 73.7 (2011): 603-606.

Anderson, James R., and Gordon G. Gallup Jr. “Which primates recognize themselves in mirrors?.” PLoS biology 9.3 (2011).

Broesch, Tanya, et al. “Cultural variations in children’s mirror self-recognition.” Journal of Cross-Cultural Psychology 42.6 (2011): 1018-1029.

de Waal, Frans BM. “The thief in the mirror.” PLoS biology 6.8 (2008).

Gallup, Gordon G. “Chimpanzees: self-recognition.” Science (1970).

Plotnik, Joshua M., Frans BM De Waal, and Diana Reiss. “Self-recognition in an Asian elephant.” Proceedings of the National Academy of Sciences 103.45 (2006): 17053-17057.

Prior, Helmut, Ariane Schwarz, and Onur Güntürkün. “Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition.” PLoS biology 6.8 (2008): e202.

Rajala, Abigail Z., et al. “Rhesus monkeys (Macaca mulatta) do recognize themselves in the mirror: implications for the evolution of self-recognition.” PLoS One 5.9 (2010): e12865.

Reiss, Diana, and Lori Marino. “Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence.” Proceedings of the National Academy of Sciences 98.10 (2001): 5937-5942.

Suddendorf, Thomas, and David L. Butler. “The nature of visual self-recognition.” Trends in cognitive sciences 17.3 (2013): 121-127.


Also interesting:

Platek, Steven M., and Sarah L. Levin. “Monkeys, mirrors, mark tests and minds.” Trends in ecology & evolution 19.8 (2004): 406-407.

Suddendorf, Thomas, and David L. Butler. “Response to Gallup et al.: are rich interpretations of visual self-recognition a bit too rich?.” Trends in cognitive sciences (2013).

Birds of a Feather

I’ve talked a lot about monkey minds on this blog, but it’s about time I got to the bird brains. Birds may have a reputation for being stupid (hence the disparaging term “birdbrain”), but they actually have some pretty incredible cognitive abilities. In fact, pigeons are one of the most widely studied animals in animal cognition labs.

320px-NZ_North_Island_Robin-2This week, though, I’m going to discuss a study that looks at cognition in a different bird, the North Island Robin of New Zealand, and in their natural habitat rather than in a lab. In this study, Barnett et al. (2013) investigated whether these birds could discriminate between familiar and novel humans.


Research has shown that birds can recognize humans who have previously approached their nests or captured them for tagging, which makes evolutionary sense: being able to recognize predators allows the birds to respond appropriately (e.g. fly away), increasing their chances for survival.

In this experiment, though, the researchers were not acting like a threat; instead of approaching the bird, a researcher placed a mealworm on the ground, then stood one meter away and timed how long it took for the bird to eat the mealworm. This encounter is likely much less stressful to the bird than if the researcher approached the bird’s nest or tried to capture it. This could actually affect the bird’s memory of the researcher because of something called the corticosterone response. When a non-human animal is stressed, its body releases corticosterone (cortisol is the human equivalent). One effect of corticosterone is to improve the formation of memories, so birds may be more likely to recognize a familiar human they’ve previously encountered in a stressful situation than one encountered in a less stressful or neutral situation.

In order to test whether the robins could discriminate between familiar and novel humans, Barnett et al. used a habituation task: they repeated the above procedure (timing how long it took for a robin to eat the mealworm) once a day for 7 days, always with the same researcher. On the 8th day, they used a different researcher.

Animals tend to be cautious when exploring novel things, so the researchers expected that the robins would be slower to eat the mealworms on the first few days. Eventually, though, they would habituate to the researcher and their “attack latency” (how long it took to eat the mealworm) would decrease. The critical data, then, is the robins’ attack latencies on the 8th day, with the new researcher. Longer attack latencies on Day 8 compared to Day 7 would indicate that the robins perceive the researcher as novel, showing that the robins can discriminate between familiar and novel humans. However, no change in attack latency on Day 8 would suggest that the robins cannot discriminate between familiar and novel humans.

But Barnett et al. were interested in more than the overall discriminative ability of North Island Robins; they also wanted to see how individual differences in behavior from bird to bird were related to this discriminative ability. Animals, like humans (although probably to a lesser extent), exhibit variations in behaviors and responses on an individual basis. The human equivalent of this is personality, although researchers also refer to it as temperament. This topic is somewhat controversial, but there are two generally accepted requirements for a behavioral trait to be considered a personality trait. First, the trait must be stable and consistent (not just a one-time behavior). Second, that trait must be related to other traits. For example, boldness, a personality trait indicating risk-taking tendency, is also related to exploratory behavior and aggressiveness.

159px-Petroica_longipes_-_Adam_Mark_Lenny_01Previous research indicates that differences in personality traits are associated with differences in learning and interacting with the environment, which is why Barnett et al. wanted to investigate individual behavioral differences in the robins. Based on the attack latency data from Day 4 (when all the animals had habituated) to Day 7, the researchers split the robins into two “behavioral types”: fast attackers and slow attackers.

The researchers found that the fast attackers did not have an increased attack latency on Day 8, suggesting that they could not discriminate between the familiar and novel researcher (or that they could discriminate between them, but didn’t perceive the novel researcher as threatening). The slow attackers, on the other hand, did have an increased attack latency on Day 8, showing that they could discriminate between the researchers. Moreover, when Barnett et al. compared the attack latencies between the two groups over all 8 days (not just Day 4 through Day 8), they found that the fast attackers habituated to the researcher on the second day, while the slow attackers didn’t habituate until the fourth day. This result agrees with previous findings that bolder animals are quicker to explore novel environments and form routines.

Barnett et al. offer a couple hypotheses of mechanisms behind these behavioral differences. Perhaps the slow learners paid more attention to their environment during the habituation phase (Days 1-7), allowing them to better perceive when the researcher was different. Another theory is that the slow attackers may have a greater corticosterone response than the fast attackers. This could cause the slow attackers to have a much better memory for the familiar researcher.

In addition to showing that North Island Robins can discriminate between familiar and novel humans, this study demonstrates that personality traits can affect individual animals’ behavioral responses. It also suggests that animal cognition researchers should take into account the personality traits of individuals when conducting cognition experiments.


Source Cited:

Barnett, Craig, et al. “The ability of North Island robins to discriminate between humans is related to their behavioural type.” PloS one 8.5 (2013): e64487.

Paying it Forward

8392492488_b3baaee68a_mYou’ve probably heard of the concept of paying it forward: someone does a small act of kindness for you and, instead of repaying that person, you pay their kindness forward by doing an act of kindness for someone else. This may not seem evolutionarily advantageous at first (the smart thing to do would be to simply accept the act of kindness and not expend energy or resources paying it forward), but remember that we are social animals. The prosocial behavior of paying it forward is beneficial to maintaining the close social ties that enable our species to survive.

So it makes sense that we might see other social animals, like non-human primates, pay it forward as well. However, many scientists think that a pay-it-forward mentality requires some higher cognitive abilities that non-human primates just don’t possess. One of these is the ability to feel and understand gratitude, which hasn’t been found in non-human primates. Social and cultural norms likely also play an important role in paying it forward. For example, if someone does something nice for you, and you don’t either do something nice back or pass it on, your reputation might suffer.

On the other hand, some scientists argue that these higher cognitive abilities aren’t required for pay-it-forward behaviors. Rather, animals could simply use generalized reciprocity (“help anyone, if helped by someone”). Generalized reciprocity is simple; it doesn’t require gratitude, or concern for one’s reputation, or taking the perspective of others, or inhibiting the impulse to look out only for oneself. So through the mechanism of generalized reciprocity, social animals without the higher cognitive abilities of adult humans can still exhibit pay-it-forward behaviors. (Why do I say “adult” humans? Because children don’t initially possess these higher cognitive abilities – they must develop them.)

160px-Cebus_apella_eating_grapes-0004Some researchers investigated whether non-human primates and human children pay it forward. Leimgruber et al. (2014) had capuchins and 4-year-old children play a game where an “actor” could choose between equal rewards for her and a “recipient”, or unequal rewards. In both cases, the reward for the actor was the same (a grape for the capuchins and 4 stickers for the children). In the equal option, the recipient received the same reward as the actor. In the unequal option, the recipient received less (spinach for the capuchins and 1 sticker for the children).

In order to see whether the capuchins and children would pay it forward, each trial of the game consisted of two rounds. In the first round, Capuchin (or Child) A would be the actor and choose the reward for herself and the recipient (Capuchin B). In the second round, Capuchin A would leave, and Capuchin B would become the new actor, who would then choose the reward for himself and the new recipient (Capuchin C).

Leimgruber et al. were interested in the choice of Capuchin B in the second round. Would he be more likely to choose the equal reward for Capuchin C if Capuchin A had chosen the equal reward for him in the previous round? Such a result would show that capuchins could indeed pay it forward.

320px-Brown_capuchin_(7958443592)The researchers found that, when the equal reward had been chosen for them in the first round, capuchins and children chose the equal reward in round two significantly more often than chance (80% and 70% of the time, respectively). Interestingly, the researchers also found that both capuchins and children also “paid forward” unequal rewards. When the unequal reward had been chosen for them in the first round, capuchins and children chose the unequal reward in round two 75% and 72% of the time, respectively.

Together, these results demonstrate that capuchins and children pass on both positive and negative outcomes (i.e. equal and unequal rewards). This suggests that, instead of a “help-if-helped” mechanism, generalized reciprocity may be more like “give-what-you-get”, where the “give” and “get” can be positive OR negative.

159px-Cebus_apella_01Leimgruber et al. suggest that the results could also be due to affective processes. “Affect” refers to basic positive and negative feelings, which have been found in many species. So, in the case of this study, receiving an equal reward could put an individual in a positive affective state, which could in turn make that individual more likely to give an equal reward in the next round. (The emotions we talk about having as humans, such as shame and the aforementioned gratitude, are considered to be secondary emotions that require higher and more complex cognitive abilities that most non-human animals don’t have.)

So does this mean that when a stranger buys my morning coffee and I pay it forward by helping my neighbor shovel his driveway, I’m influenced by “give-as-you-get” or a positive affective state? Probably not, say the researchers. Adult humans do have concern for their social reputations, can feel gratitude, and can take the perspectives of others, and we are likely greatly influenced by these considerations. But the simple “give-as-you-get” mechanism and the effect of affect form the base upon which these considerations build, allowing humans to make complex social decisions and have incredibly rich social relationships.

Sources Cited:

Leimgruber, Kristin L., et al. “Give What You Get: Capuchin Monkeys (Cebus apella) and 4-Year-Old Children Pay Forward Positive and Negative Outcomes to Conspecifics.” PLOS ONE 9.1 (2014): e87035.

van Doorn, Gerrit Sander, and Michael Taborsky. “The evolution of generalized reciprocity on social interaction networks.” Evolution 66.3 (2012): 651-664.

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.