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What do capuchin monkeys feel when they take risks?

Emotion and cognition have traditionally been viewed as separate entities. Only recently has empirical research examined the role of emotions in decision making. In human beings, all decisions have affective consequences that can, in turn, impact subsequent decisions. In nonhuman animals, ,still little is known about the role of emotional responses on decision making. In a new study of the Unit of Cognitive Primatology, published on Animal Behaviour, researchers analyzed behavioral indexes of negative emotions, like scratching or hiccup vocalizations, in capuchin monkeys during a risky choice task. In this task, monkeys have to choose between a safe option (always constant) and a risky option that corresponds to a better or a worse prize. They found that capuchins show more negative emotions after choosing the risky option and receiving the worst prize than when they receive the better one. Moreover, capuchins try to switch their choice more often after receiving the worse prize than the good prize, a phenomenon known as "regret" in humans.

Video clip 1. Neutral condition. Robin hood, a male capuchin, is presented with the choice between a safe option (four food items covered by the white bowl, on the experimenter’s right) and a risky option (in this case, one food item covered by the red bowl, on the experimenter’s left). He chooses the risky option by inserting his finger in the hole of the corresponding transparent box, the experimenter provides him with the corresponding food reward (one food item) and Robin hood shows scratching behaviour.

Video clip 2. Disadvantageous condition. Gal, a male capuchin, is presented with the choice between a safe option (four food items covered by the yellow bowl, on the experimenter’s left) and a risky option (in this case, one food item covered by the pale blue bowl, on the experimenter’s right). He chooses the risky option by inserting his finger in the hole of the corresponding transparent box, the experimenter provides him with the corresponding food reward (one food item) and Gal shows switching behaviour (i.e., he inserts his finger in the hole of the previously non-selected box). 

Capuchins prefer risky gambles over a safe reward

Pathological gambling affects 0.2% to 5.3% of adults in western societies, is highly comorbid with a range of other psychiatric disorders and with substance abuse, and is associated with increased suicidal ideation and attempts compared to the general population. In view of the growing incidence of pathological gambling and its severe mental and social consequences, it is urgent to further deepen our understanding of the neuronal and psychological underpinnings of this condition. Laboratory studies on nonhuman primates can inform the research on human pathological gambling in several ways. 

The comparison of risk preferences between phylogenetically closely related nonhuman primate species with different ecologies can shed light on the selective pressures that shaped decision-making under risk in the course of the evolution. We presented 10 capuchin monkeys with choices between a "safe" option (always four food items) and a "risky" option (either one or seven food items) in three conditions differing for the probability of receiving the larger outcome when selecting the risky option (66%, 50% and 33%, respectively). When the probabilities of obtaining the larger outcome were 66% and 50% capuchins were risk prone, but when the probability was lowered to 33% they flexibly modified their preferences becoming indifferent to risk. Capuchins’ decision-making under risk mirrors their risk-prone behaviour in the wild, where they often rely on unpredictable and/or hazardous food sources. 

The video shows Robin hood, a male capuchin, presented with the choice between a "safe" option (four food items covered by the white bowl) and a "risky" option (either one or seven food items with 50% probability, covered by the red bowl; in this case, one food item). He chooses the "safe" option by inserting his finger in the hole of the corresponding transparent box and the experimenter provides him with the food.

Sometimes, to be patient pays off

Is a bird in the hand worthier than two in the bush? Ask a capuchin and he might probably prefer two birds in the bush. When choosing between two rewards, giving that the favorite one is not immediately available, capuchins are willing to wait to obtain their preferred recompense. Indeed, they show a high tolerance to delay.

Both human and non-human animals often face decisions between options available at different times, in the animal world the capacity of delaying gratification has usually been considered one of the features distinguishing humans from other animals. However, this characteristic can vary across individuals, species, types of task, and it is still unclear whether it is accounted for by phylogenetic relatedness, feeding ecology, social structure, or metabolic rate.

To disentangle these hypotheses, we carried out an experiment to evaluate temporal preferences in capuchin monkeys. We gave capuchins the opportunity to choose between two food quantities (two versus six pieces of peanuts), the smallest was immediately available, the other delayed. It came out that subjects could wait up to two minutes in order to obtain the bigger reward. Overall, capuchins possess a significantely higher delay tolerance than closely related species, such as marmosets and tamarins, and that is likely to be compared to that shown by great apes. Capuchins’ tool use abilities might explain their comparatively high preference for delayed options in inter-temporal choices. Moreover, as in humans, capuchin females showed a greater delay tolerance than males, possibly because of their different fraging style. Males are more opportunistic than females: they spend more time on the ground foraging for exposed large invertebrates and small vertebrates, while females remain a few meters above the ground searching for small and embedded invertebrates. Thus, it is possible to explain the evolutionary origins of delay tolerance (or self-control) in terms of feeding ecology.

Video above. Paprica, a female capuchin, has to choose between a smaller immediate reward (two pieces of food, on the left) and a larger delayed reward (six pieces of food, on the right). When Paprica selects the larger delayed reward by inserting her finger in the hole of the box containing the food, the experimenter removes the non-chosen smaller reward, and – after a delay of 10 seconds – she pushes the sliding panel with the six pieces of food towards the capuchin. 

To be self-controlled is much more easier when you do are not dealing with real objects, but with their symbolic representations. We carried out an experiment to see if symbolic artifacts such as tokens would inhibit capuchins’ strong behavioral predisposition, as occurs in children and chimpanzees. In our experiment, monkeys had to choose between two food quantities or two tokens, representing respectively the smaller and the larger food quantity. In all conditions, subjects had to select the smaller quantity (or the low-value token) to obtain the larger reward (or the amount of food corresponding to the high-value token). Symbolic artifacts did improve performance: most of the subjects succeeded with tokens, while only one succeeded with food. Thus, tokens allowed capuchins to achieve psychological distancing from the incentive features of food, leading them to avoid impulsive choices in favour of more advantageous alternatives.

Videos from Addessi & Rossi 2010 Proc. R. Soc. B-Biological Science:

Experimental phase - FOOD-condition.

Sandokan, a male capuchin, has to choose between five units of food (on the right) and two units of food (on the left). He makes the wrong choice, since he selects the larger amount of food and thus receiving in this way the non-chosen smaller amount of food as reward.

 

Experimental phase - LSDT-condition. Robinia, a female capuchin, has to choose between five low-symbolic distance tokens (on the left) and two low-symbolic distance tokens (on the right). Each low-symbolic distance token is worth one unit of food. Robinia correctly chooses the smaller amount of low-symbolic distance tokens, and receiving five units of food as reward, i.e. the amount of food corresponding to the non-chosen five low-symbolic distance tokens.

 

Experimental phase - HSDT-condition.

Sandokan, a male capuchin, has to choose between two high-symbolic distance tokens: a blue chip, worth two units of food (on the left) and a metal strip, worth five units of food (on the right). He correctely chooses the blue chip and thus receiving five units of food as reward, i.e. the amount of food corresponding to the non-chosen metal strip.  

Are capuchins indeed so patient?

In the Delay choice task subjects are presented with a choice between a smaller immediate option and a larger delayed option. This task is frequently used to assess delay tolerance, interpreting a preference for the larger delayed option as willingness to wait. However, recent data show that this might not be always the case. 

In the Delay choice task subjects face a dilemma between two preferred responses: “go for more” (i.e., selecting the larger, but delayed, option) vs. “go for sooner” (i.e., selecting the immediate, but smaller, option). When the options consist of visible food amounts, at least some of the choices of the larger delayed option might be due to a failure to inhibit a prepotent response towards the larger option rather than to a sustained delay tolerance. To disentangle this issue, we tested 10 capuchin monkeys, 101 preschool children, and 88 adult humans in a Delay choice task with food, low-symbolic tokens (objects that can be exchanged with food and have a one-to-one correspondence with food items), and high-symbolic tokens (objects that can be exchanged with food and have a one-to-many correspondence with food items). This allows evaluating how different methods of representing rewards modulate the relative contribution of the “go for more” and “go for sooner” responses. Consistently with the idea that choices for the delayed option are sometimes due to a failure at inhibiting the prepotent response for the larger quantity, capuchins and children chose the larger delayed option more with food than with high symbolic tokens, whereas low-symbolic tokens were ineffective in decreasing the salience of the larger option. Conversely, the sophisticated symbolic skills of adult humans prevented the distancing effect of high-symbolic stimuli in this population. Thus, at least in capuchins and children, opting for the larger delayed option in the visible-food version of the Delay choice task seems to partially result from an impulsive preference for quantity, rather than from a sustained delay tolerance. Our data extend the knowledge concerning the influence of symbols on both human and non-human primate behavior and invite greater caution in interpreting the results obtained with the visible-food version of the Delay choice task, which may overestimate delay tolerance. The above findings are supported by the lack of correlation between the performance in the Delay choice task and in other tasks measuring delay tolerance in non-human primates, children, and adults. 

Capuchins set the right value on things

If capuchins were to choose between one piece of good food and two pieces of a low-quality one, it is not so sure they will take the larger quantity. As humans, in fact, monkeys understand the difference between quantity and quality, and their choices depend mainly on the relative value they assign to things.

Apart from humans, monkeys are able to make rational and economically advantageous choices based on the relative value of things. We studied economic choice behavior in capuchin monkeys by offering them to choose between two different foods available in variable amounts. When monkeys select between familiar foods, their choice patterns are well-described in terms the relative value of the two foods. In other words, they choose not only to take into consideration the quantity, but also the quality of the resources.

The same results emerged when capuchins had to select foods they have never tasted before: they learned to choose between them gradually, assigning each food a specific value. This result demonstrates that capuchins’ choices are not based on a stimulus-response association acquired through experience, as the leading view in economics and biology uphold. We propose instead a cognitive model in which the economic choice is the result from a two-stage mental process characterized by two different stages: of value-assignment and decision-making.

 

In the video Robin hood, an adult capuchin male, presented with a choice between two small raisins (on the left) and one large piece of banana (on the right), selects the two raisins.

Decision making and tool use

Wild bearded capuchins (Sapajus libidinosus) are small bodied primates. Adult females weight about 2 kg while adult males weigh about 3.5 kg (the dominant male being more than 4 kg). The most resistant palm nuts they break with tools are about 20 times harder than walnuts, whereas the resistance of other palm nuts is only about 10 times that of walnuts.Therefore, no doubt that the use of heavy stones is especially advantageous when the capuchin has to break hard nuts. However, if the heavy stone needs to be transported to the anvil then ... the monkey faces a high cost of transport.

What capuchins decide to do when faced with a heavy stone far from the anvil and a light stone close to the anvil? is theur decisional process affected by the resistance of the nut they need to crack open?

To assess the role of stone mass and transport distance in capuchins' tool selection, Massaro and colleagues (2012) carried out a series of field experiments. Overall, they demonstrated that all things being equal capuchins minimize transport distance choosing the closest stone to the anvil. However, when the nut is very resistant and there are a light stone is on the anvil and a heavy stone farther away, capuchins transport to the anvil and use only the latter. In contrast, when the nut is less resistant capuchins use both stones. 

Overall, individuals vary in their sensitivity to distance of transport, a few meters are perceived as a substantive cost by some monkeys, and individuals' body mass affects decision making.

 

Researcher involved

Dr. Elsa AddessiDr. Elisabetta Visalberghi

Dr. Francesca De Petrillo

Dr. Serena Gastaldi

 

ico Bullet Scientific publications 

ico Bullet Capuchins and media

 

 

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