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.


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).

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.

What’s in a Face?

3008056718_0162d2e2c4_mUndoubtedly the scariest time of year (besides maybe tax season) is Halloween – as October rolls around, we pause our perpetual avoidance of fear and instead embrace it, reveling in haunted houses and scary costumes. But how do we know what scary is, and why are many things universally frightening? Part of the answer could be cultural: for example, the mask from Scream or the hooded, scythe-wielding Grim Reaper. There could also be evolutionary influences on what we find frightening, such as sharp teeth and grotesque facial features.

Some scientists have approached this question from the field of face perception. They ask a more specific question: What makes a face scary? Previous research on face perception has examined the ability of humans (and, amazingly, some animals) to detect distorted faces, and has gauged preferences for attractive faces over unattractive ones. Sinnott et al. (2012) took this latter line of research further to investigate how animals and humans perceive scary faces – in particular, scary Halloween masks.

They began with three hypotheses about how non-human animals might react to the masks:

1. Human Cultural Hypothesis – Faces are scary not because of any particular way they look, but because of the cultural meaning associated with them. So a skull is scary because we associate it with death, the Scream face is scary because of its associations with the horror film, etc. If this hypothesis is true, we would expect animals to be unaffected by the masks, compared to humans.

2. General Biological Hypothesis – Many scary masks possess features commonly associated with predators, such as sharp teeth and large, angry eyes. This hypothesis predicts that animals would therefore perceive the masks as predators and be frightened of them.

3. Primate Biological Hypothesis – Primates have more complex faces than other animals – they can move facial features independently of each other to make various facial expressions, and they can use those expressions as way to communicate emotions like aggression and fear. Nonhuman primates thus may be more likely than other animals to perceive the frightening nature of the masks. If this is the case, then non-human primates, but not other animals, should be frightened of the masks.

In order to test these hypotheses, Sinnott et al. studied the avoidance response latency for animals to take food from a masked experimenter. In each trial, an experimenter wearing a mask offered an animal some food, then measured the amount of time the animal hesitated before taking it. If an animal is frightened, it will be more cautious and hesitate longer before taking the food. On the other hand, an animal unaffected by the mask will take the food with little or no hesitation.

Sinnott et al. tested 13 different Halloween masks, ranging from politicians to vampires to aliens. They also conducted control trials, where the experimenter was unmasked, to rule out the possibility that the animals were frightened by humans in general. They tested a wide variety of animals, including several primate species, lions, a bear, a camel, and macaws.

Screen Shot 2013-11-06 at 11.04.54 AM

The 13 masks used by Sinnott et al., plus a picture of the unmasked experimenter. (Source: Sinnott et al. 2012)

They found that primates had significantly longer response latencies than non-primates for all masks. There was no difference between primate and non-primate latencies in the control trials, ruling out the possibility that the primates were just more afraid of humans. Since only the primates were affected by the masks, Sinnott et al. rejected the General Biological Hypothesis, which posits that all animals should be frightened by the masks.

The fact that the non-human primates had longer response latencies suggests that the Human Cultural Hypothesis may also be incorrect, but Sinnott et al. wanted to directly compare non-human primates and humans by investigating whether they found the same masks to be scary. They asked humans to rate the masks on a scale of 1 (not scary) to 7 (very scary). When they compared those ratings to the non-human primates’ response latencies, they found a significant correlation – in general, non-human primates were more afraid of (had longer response latencies for) the masks that humans rated as scarier! This supports the Biological Hypothesis – the primates perceive the frightening nature of the masks, probably due to their greater sensitivity to facial expressions.


Example of a fear grimace

There were a couple interesting differences in how non-human primates and humans perceived the masks. For example, the non-human primates had longer response latencies for the politician masks, which the humans rated as not very scary. Sinnott et al. suggest that this is because the politician masks have big, toothy smiles, which the non-human primates likely perceive as “fear grimaces” (a smile-like baring of teeth that indicates fear).

The results of this study suggest that some higher-level cognitive process occurs in the primate brain when perceiving the scary masks (and probably faces in general). The presence of predator-like facial features (like big teeth) alone isn’t sufficient to elicit fear, or else all the animals would have been affected by the masks. Rather, primates may interpret what they perceive at a higher cognitive or even emotional level, which causes them to fear a face (or not).

So although humans may find some faces scary due to cultural associations, there’s also likely an evolutionary influence on the scariness of a face, based on facial features and their configuration, and requiring higher emotional and cognitive processes.

After all that talk about fear, I’ll end this post on a fun note: here’s a video showing how the animals at the London Zoo celebrated Halloween this year. Zoos often use holidays and birthdays as opportunities to provide the animals with themed enrichment (new and interesting things to explore and eat!).


Sinnott, Joan M., et al. “Perception of Scary Halloween Masks by Zoo Animals and Humans.” International Journal of Comparative Psychology 25 (2012): 83-96.

Will Work for (Equal) Pay

Scales_of_Justice_(PSF)One important concept we possess at a young age is fairness (as any parent of multiple children will confirm!). Children especially do not hesitate to speak up (or, more often, whine) if they detect inequality, and much of our society focuses on achieving fairness for all. Given the sociality of some animal species, could these animals also have a concept of fairness?

Brosnan & de Waal (2003) investigated whether capuchin monkeys (who are considered very social) conceptualize fairness. (The term most researchers use is “inequality aversion”, since they’re not sure if it is actually the same as the human concept of fairness. For simplicity, I’ll continue to call it “fairness”.) They first taught the capuchins an exchanging task, where the researcher gives the monkey a token (e.g. a rock), which the monkey then hands back to the researcher in exchange for a treat.

Once the capuchins learned this task, Brosnan & de Waal wanted to see how they would react to getting a less desirable treat than another capuchin in the same task. It seems obvious that they would be upset – they’re doing the exact same task as the other capuchin, so they should also get the more desirable treat (equal “pay” for equal “work”). But think about the thought processes required for such a reaction: the capuchin must not only pay attention to the task the other capuchin does, but also recognize that it is the same task she does. Then she has to see what treat the other capuchin gets, and then realize that it is better than the treat she gets. Finally, and most importantly, she has to CARE about that disparity – this is what we call fairness (and what researchers call inequality aversion).

In order to study fairness in capuchins, Brosnan & de Waal did the exchange task with two capuchins that were in separate, side-by-side enclosures. There were no opaque barriers between the enclosures, so capuchins could clearly see each other doing the task. In the inequality condition of the exchange task, one of the capuchins would always receive a grape (a more preferred treat), and the other capuchin would always receive a piece of cucumber (a less preferred treat). As a control, the researchers also conducted sessions of the task where both capuchins got the same treat.

small__5546971563Brosnan & de Waal found that in the inequality condition, the capuchin receiving the cucumber often refused to do the exchange task, either by refusing to return the token or refusing to take the treat (here’s a short clip showing a hilarious example of this – I highly recommend watching it!). These “non-exchanges” occurred on about 40% of trials in the inequality condition, but only about 5% of trials in the control condition (when both capuchins got the same treat). So when the researcher wasn’t playing fair, the cheated capuchin often refused to play at all!

The researchers decided to do the same task, but with an even bigger disparity. This time, instead of merely giving the capuchins unequal pay for equal work, the capuchin receiving the grape didn’t have to work for it at all – she was just given the grape, while the other capuchin still had to exchange for the cucumber. In this condition, non-exchanges by the cucumber capuchin increased to around 80% of trials!

The results of these two experiments suggest that capuchins do have some concept of fairness, though it may not be exactly like the concept of fairness that humans have. In a final experiment, Brosnan & de Waal investigated the effect of the mere presence of a grape on the cucumber capuchin’s reaction. They tested only one capuchin at a time, making her exchange for a piece of cucumber, and placing a grape in front of the (empty) adjacent enclosure. The results were similar to the first experiment: the capuchin refused to exchange in about 40% of the trials.

This suggests that their concept of fairness may not require equal treatment relative to other capuchins. Rather, their concept may only require that a better reward exists, regardless of whether another capuchin is receiving that reward.

Overall, these results suggest that some kind of concept of fairness may be innate in primates (including humans). However, evolutionarily, the capuchins’ behavior seems a bit puzzling: If you’re trying to survive, you should take whatever food you can get, rather than refuse it because something better exists (especially if you wouldn’t get that better food anyway). How could this behavior be evolutionarily advantageous? (Hint: Think about why the researchers did this experiment with capuchins in the first place.)

A lot of work research on fairness in primates has been done since Brosnan & de Waal published their results. Here’s a recent review of that literature, for those who are interested (unfortunately, the article isn’t available for free, but hopefully those affiliated with a university or research institute can access it).

(The clip I linked to above is taken from de Waal’s fascinating TED Talk on moral behavior in animals – check it out!)


Brosnan, Sarah F., and Frans BM De Waal. “Monkeys reject unequal pay.” Nature 425.6955 (2003): 297-299.